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Neuromorphic Devices

2D MoS2 Neuromorphic Devices for Brain-Like


Computational Systems
Jie Jiang, Junjie Guo, Xiang Wan, Yi Yang, Haipeng Xie, Dongmei Niu, Junliang Yang,
Jun He,* Yongli Gao, and Qing Wan*

Hardware implementation of artificial synapses/neurons with 2D solid-state devices


is of great significance for nanoscale brain-like computational systems. Here, 2D
MoS2 synaptic/neuronal transistors are fabricated by using poly(vinyl alcohol) as the
laterally coupled, proton-conducting electrolytes. Fundamental synaptic functions,
such as an excitatory postsynaptic current, paired-pulse facilitation, and a dynamic
filter for information transmission of biological synapse, are successfully emulated.
Most importantly, with multiple input gates and one modulatory gate, spiking-
dependent logic operation/modulation, multiplicative neural coding, and neuronal
gain modulation are also experimentally demonstrated. The results indicate that the
intriguing 2D MoS2 transistors are also very promising for the next-generation of
nanoscale neuromorphic device applications.

Today digital computers are based on vvon Neumann archi- increasingly inefficient when it meets complicated computa-
tecture, where the memory and processor are physically tion or real-time processing of visual/speech recognition.[1]
separated. Despite the great achievements made so far, In contrast, the human brain consists of ≈1011 neurons, and
this conventional von Neumann architecture is becoming each neuron is connected with adjacent neurons through
103–104 synapses.[2] It is a highly parallel, fault-tolerance,
energy-efficient, and event-driven information processing
Prof. J. Jiang, J. Guo, Dr. H. Xie, Prof. D. Niu, system, which is fundamentally different from the conven-
Prof. J. Yang, Prof. J. He, Prof. Y. Gao
tional von Neumann computer.[2] Therefore, an emerging
Hunan Key Laboratory of Super Microstructure
and Ultrafast Process field of brain-inspired neuromorphic computing is proposed
School of Physics and Electronics to break this von Neumann bottleneck, which takes the
Central South University advantage of massive parallelism that comes from distributed
Changsha, Hunan 410083, China computing and localized storage in networks.[3–7]
E-mail: junhe@csu.edu.cn As a key element in the human brain, each synapse con-
Dr. X. Wan, Dr. Y. Yang, Prof. Q. Wan nects two adjacent neurons, and its synaptic strength (weight)
School of Electronic Science and Engineering and Collaborative can be precisely adjusted by the concentrations of ionic spe-
Innovation Centre of Advanced Microstructures
cies, such as Ca2+, Na+, Mg+, etc.[2,8,9] Synaptic plasticity is a
Nanjing University
Nanjing 210093, China general mechanism that regulates the experience-dependent
wanqing@nju.edu.cn change in connectivity between neurons, and it is believed
Dr. X. Wan, Dr. Y. Yang, Prof. Q. Wan to underlie learning and memory of the biological brain.[9]
Key Laboratory of Microelectronic Devices and Integrated Technology Thus, the hardware implementation of biological synapses
Institute of Microelectronics with solid-state devices is of utmost importance for realizing
Chinese Academy of Sciences brain-inspired computational systems and real-time brain
Beijing 100029, China simulators. Historically, solid-state synapse elements have
Prof. Y. Gao been emulated by silicon-based metal-oxide-semiconductor
Department of Physics and Astronomy
(CMOS) circuits using tens of transistors.[10,11] However, this
University of Rochester
Rochester, NY 14627, USA
approach consumes a substantial area and energy on the
chip, which is not feasible for large-scale integration. In the
DOI: 10.1002/smll.201700933 past few years, different kinds of two-terminal emerging

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memory that show an electrically triggered resistive switching importance. However, up to now, synaptic plasticity modula-
phenomenon have been proposed for artificial synaptic tion through an electric field is to be investigated in the 2D
devices that can be programmed in an analog fashion, such MoS2 materials. In this work, such synaptic plasticity modula-
as Ag2S- or Cu2S-based atomic switches,[3,12,13] Ge2Sb2Te5- tion can be successfully implemented by the novel electric-
based phase-change memory,[14] metal-oxide-based resistive double-layer gating approach. Such important device physics
switching memory,[1,15–17] etc. Using these artificial elements, can be further developed for more advanced synaptic/neu-
some synaptic behaviors, like synaptic plasticity, spike-timing- ronal neuromorphic computing, such as an excitatory post-
dependent plasticity (STDP), and self-learning ability, have synaptic current (EPSC), paired-pulse facilitation (PPF), and
been successfully emulated. More recently, three-terminal dynamic filter. Most importantly, with multiple presynaptic
devices have been proposed as artificial neuromorphic syna­ inputs, spiking-dependent logic operation/modulation, mul-
pses for emulating biological synaptic functions. Several tiplicative neural coding, and neuronal gain modulation for
groups have reported the three-terminal artificial synapses by spatiotemporally correlated signal processing of biological
using carbon nanotube transistors,[18] nickelate-based transis- neurons are emulated in such a neuromorphic device. Such
tors,[19] and oxide-based transistors,[20–22] respectively. Typical a neuromorphic demonstration in a MoS2-based device
synapse functions, such as dynamic logic, self-learning, STDP, can represent a great step toward next-generation, smart,
etc., have been successfully demonstrated with these three- nanoscale electronic devices with artificial intelligence, such
terminal artificial synaptic/neuron devices. Such devices can as smart machines and man–machine interfaces.
greatly broaden artificial synaptic electronics to overcome The insets of Figure S1a (Supporting Information)
the limitations of previous materials and device architecture, exhibits the molecular structure of the PVA membrane and
which provides a new way to realize neural networks and a sandwiched metal/PVA/metal structure for measuring the
brain-like neuromorphic computation. PVA capacitance, respectively. Figure S1a (Supporting Infor-
At the same time, as the traditional semiconductor scaling mation) shows frequency-dependent specific capacitances
closes to its physical limits, atomically layered 2D materials (Ci) of the PVA membrane, with the frequency ranging from
have attracted growing interests since the first discovery of 1.0 Hz to 100 kHz. The Ci exhibits a low value of 1–3 nF cm−2
graphene in 2004 and the later Nobel Prize of Physics in 2010, at high frequency in the domain of 70 Hz to 100 kHz, then
respectively.[23–31] Compared to zero-band-gap graphene, MoS2 increases with decreasing frequency, and finally reaches to a
is recently considered as one of the most promising 2D mate- maximum value of ≈2 µF cm−2 at 1.0 Hz. Such a high capaci-
rials for replacing the widely explored 2D graphene, because tance is due to the mobile-ions-induced EDL effect,[44–46]
it is a semiconducting, 2D layered transition-metal dichalcoge- which will be discussed later. Figure S1b (Supporting Informa-
nide, with a band gap changing from 1.2 eV in the bulk to 1.8 eV tion) shows the leakage current curves of the PVA film in the
in monolayers.[32–34] With these intriguing electronic and optical voltage range from −1.5 to 1.5 V. The maximum leakage cur-
properties, and special atomically scalable structure advantages, rent is only ≈0.5 nA during this measurement. Interestingly,
the 2D MoS2-based devices exhibit high promise for many at zero voltage, there is an offset in the current (in both direc-
state-of-the-art electronic applications, such as photovoltaic tions), which indicates that amounts of charged ions (i.e., an
solar cells,[35,36] flexible electronics,[37,38] advanced ultrasmall internal electric field) are present in the PVA membrane, and
transistors,[39,40] integrated circuits,[41,42] etc. Recently, we note its slow response to the external bias finally results in a signifi­
that Arnold et al. have reported an interesting work to mimic cant clockwise hysteresis. It is to be noted that the transient
neurotransmitter release by using interface trapping/detrap- leakage current is associated with the ionic migration, which
ping in MoS2 transistors.[43] The authors argue that the trap- is directly depended on the external voltage magnitude.[47,48]
ping/detrapping mechanism is depended on ambient water and If the external voltage is small, the EDL gating process is
oxygen molecules adsorption/desorption. Although this work is corresponded with the “electrostatic modulating process”,
of great interest, the underlying mechanism may limit its poten- and the leakage current is accordingly small. However, if
tial neuromorphic applications (need the ambient water and the external voltage is relatively large, the EDL gating pro-
oxygen molecules). Therefore, up to now the 2D MoS2-based cess is corresponded with the “electrochemical doping pro-
neuromorphic device still remains largely unexplored. cess”, and the leakage current becomes large. In this work,
In this Communication, for the first time, proof-of-prin- the applied gate voltage during the measurements is limited
ciple neuromorphic devices with multiple presynaptic inputs within 1.5 V, which results in an acceptable leakage current
are proposed based on a poly(vinyl alcohol) (PVA) proton- (≤0.5 nA). Most importantly, we use a solid organic electro-
conducting electrolyte, laterally coupled, 2D MoS2 electric- lyte, poly(vinyl alcohol), in this work, rather than a traditional
double-layer (EDL) transistor. The choice of MoS2 in this liquid electrolyte, which usually has a large leakage current
work lies in two reasons: First is the growing interest in 2D due to its liquid nature. These two reasons can guarantee that
layered semiconductors as promising candidates for future the leakage current during the measurements does not have a
solid-state nanodevices due to their atomically thin body significant effect on the device performance. Figure S1c (Sup-
that allows for aggressive scaling and excellent electrostatic porting Information) shows the X-ray photo­electron spec-
control. Second, and most importantly, in this attractive 2D troscopy (XPS) C1s core levels of the PVA membrane. The
nanoscale community, an artificial intelligence based on 2D synthesized profiles (black line) are overlaid on the experi-
neuromorphic synaptic device is still lacking. Therefore, we mental data (black dot). The C1s spectra can be well fitted
develop the atomically layered MoS2 as a channel material by four peaks, which are indicated by colored lines. There
in the synaptic device, which is of great significance and high are two prominent peaks corresponding to the CH2 group

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(285.0 eV) and the alcoholic CHOH group (286.5 eV).[49] the neuromorphic computation. Although the EDL transistor
The remaining two peaks are the CO group (287.8 eV) may have the issue of low-frequency operation, we note that
and amorphous carbon (284.5 eV), which may be ascribed in a human brain the typical frequency of neural activities is
to environmental carbon contamination during the sample just within the low-frequency domain (1–30 Hz). It is the ion
preparation and/or subsequent X-ray-induced transforma- movements (electric/chemical process) that play a central role
tion in the XPS measurement.[49,50] Figure S1d (Supporting in the neural activities of the human brain, such as synaptic
Information) further shows the Fourier transform infrared integration and neuronal computation. Therefore, although
spectroscopy (FTIR) of the PVA membrane. From this the EDL gating would make the device slow, it is reasonable
figure, it clearly reveals the major peaks associated with the and acceptable for some specific applications, especially for
PVA membrane. For instance, the most prominent peaks are some low-frequency applications such as the artificial neuro-
linked to CH stretching at 2930 cm−1 and OH stretching morphic electronics in this work (that is to say, to mimic the
at 3432 cm−1, respectively.[51,52] Intramolecular and inter- synaptic/neuronal computation by using such a solid device).
molecular hydrogen bondings are expected to occur among Figure 1a shows the schematic picture of the 2D, proton
PVA chains due to high hydrophilic forces. The remaining conducting, PVA-coupled MoS2 transistor. A coplanar
two peaks from 1096 to 1637 cm−1 are originated from the late­ral gate is coupled with a 2D layered MoS2 channel by
CO stretching and CO stretching, respectively.[51,52] These a PVA-based proton conductor. A top-view optical image of
results are very consistent with the XPS measurements. Based the completed device can be shown in Figure 1b. It exhibits
on the above results, a proton-conducting mechanism can be a clear image where two gold electrodes are bridged by a
proposed in the hydrogen-bond-rich polymers. As shown in MoS2 flake, and a lateral gate is located near the MoS2 flake
the inset of Figure S1d (Supporting Information), through in the same plane. The thickness of the MoS2 flakes can be
a Grotthuss mechanism, the sequence of proton hopping measured by atomic force microscopy (AFM). As shown in
occurs between hydroxyl groups and water molecules under Figure S2a (Supporting Information), a MoS2 flake with a
an external electric field.[44,53–56] Therefore, accumulation thickness of ≈6.5 nm is observed in our device. Based on a
of mobile protons at the PVA/metal interface would result 0.65 nm thickness per layer value,[32] the number of layers in
in a large EDL capacitance, and thus a strong electric-field this MoS2 flake should be ≈10 layers. The inset in Figure S2a
coupling effect, which is very helpful to realize the artificial (Supporting Information) shows a schematic picture of lay-
synaptic electronics. Here, it should be noted that compared ered atomic structure for MoS2 flake whose structure is com-
to the traditional dielectrics like Al2O3 or HfO2 or h-BN (all posed of stacks of layers separated by van der Waals forces.
of them do not have enough charged ions), the EDL electro- Figure S2b (Supporting Information) shows the Raman
lyte has many mobile charged ions, which is helpful to realize spectra of the exfoliated MoS2 samples tested in dark and

Figure 1.  a) A schematic picture of the 2D MoS2 synaptic transistor. b) A top-view optical image of the completed device. c) Transfer curve of the
MoS2 transistor with a fixed bias of VDS = 0.1 V. d) The corresponding output curve of MoS2 transistor.

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air ambient environment. Two major peaks are located at signals from the preceding nodes and then transmits it to the
≈384 and ≈409 cm−1, which correspond to the E 12g and A1g next layer.[4] Normally, the node can provide an adding for
modes,[57] respectively. Vibration of the E 12g mode involves the the presignals, which are scaled with weight (i.e., synapse).
in-plane opposing motions of sulfur and molybdenum atoms, Following this, the output of the node corresponds to the sum
and that of the A1g mode is the out-of-plane relative motions of input signals. Interestingly, the neural functionality in such
of sulfur atoms,[57] as shown in the insets of Figure S2b (Sup- neural network can be generally expressed with the synaptic
porting Information). The transfer characteristics (IDS – VGS) weights, which can be modulated in biological processes.[4]
with a fixed bias of VDS = 0.1 V in linear region (VGS − VTH > Figure 2b shows a magnified schematic diagram for two adja-
VDS) is shown in Figure 1c by sweeping the VGS from −1.5 to cent neurons with a synapse, which is a key element in neural
1.5 V and then sweeping back again. During all of our measure- network of human brain. For a typical synaptic connection,
ments, we set a constant and small bias of VDS = 0.1 V. This small neurotransmitters are released from the presynaptic neuron
and constant voltage is used to “read” the postsynaptic current into the synaptic cleft when an action potential arrives.[2,8,9]
and meanwhile avoid the coupling of VDS with VGS. From this These neurotransmitters can diffuse across the synaptic
figure, it is clear that the device can operate at a low voltage cleft, then couple with the receptors in the post-neuron,
(1.5 V) and exhibit high current on-off ratios (Ion/off > 104). and finally trigger a subsequent action potential in the post-
Interestingly, the device shows a clear anticlockwise hyster- neuron. Similar to this architecture, our artificial 2D MoS2
esis, which may be ascribed to the presence of mobile pro- synaptic transistor uses the coplanar lateral gate as the pre-
tons in the PVA polymer. As shown in Figure 1d, the typical synaptic input terminal and 2D ultrathin MoS2 channel with
output curve can be measured by sweeping the VDS from 0 source/drain electrodes as the postsynaptic output terminal.
to 1 V with a fixed VGS from −1 to 1.5 V in 0.5 V steps. Good Figure 2c shows the typical EPSC of 2D MoS2 synaptic tran-
pinch-off characteristics and excellent linear character are sistor triggered by a presynaptic spike (1 V, 10 ms). A VDS of
observed in the high VDS and low VDS regimes, respectively. 0.1 V was applied between the source and drain electrode for
Such good pinch-off characteristics are due to a strong gate- EPSC measurement. A peak value of EPSC ≈ 23.6 nA was
modulation by the EDL electrolyte, because the typical observed at the end of the spike where it gradually decayed
operation voltage of traditional MoS2 transistor with bottom- back to the resting current (≈0.4 nA) in ≈300 ms. Such EPSC
gated, thermal-grown SiO2 dielectric is usually more than behavior is quite similar to the EPSC process in a biological
20 V, while the operation voltage of this device is below 1.5 V. excitatory synapse.[2] Here, we should note that the transfer
These results strongly indicated that it is a typical polymer– curve of MoS2 transistor with liquid pure water as the gate
proton–conductor-gated 2D transistor and is very meaningful dielectric shows the similar anticlockwise hysteresis with the
for artificial synapse. Here, we should point out that the dis- PVA-gated device, as shown in Figure S4a (Supporting
tance between the channel and the gate electrode should Information). To further examine the effect of water on
affect strongly to the operational speed of the device. To the neuromorphic operation of MoS2 transistor, the EPSC
address this issue in our proton-conducting neuromorphic response of MoS2 neuromorphic transistor was measured
device, frequency-dependent phase angle measurements are by triggering a presynaptic spike (1 V, 10 ms), as shown in
performed with different distances between the channel and Figure S4b (Supporting Information). However, the peak
the coplanar gate (Dchannel-gate = 30, 60, 90 µm, respectively). value of EPSC recovered to its original value within a short
As shown in Figure S3a (Supporting Information), it is evident time (<10 ms) at the end of the spike, compared to the PVA-
that at the low frequency the phase angle changes from −45° gated MoS2 transistor. The reason may be due to the lack of
(more capacitive) to −30° (more resistive) when the Dchannel-gate enough charged ions inside the pure water, while the number
increases from 30 to 90 µm, which implies that the ion migra- of charged ions in PVA solution is much more. At the same
tion does not have enough time to response for Dchannel-gate = time, it should also be noted that synaptic plasticity due to
90 µm (compared to Dchannel-gate = 30 µm). We can define a long-term potentiation occurs at a much longer timescale than
critical frequency (f) at the phase angle of −45°. It is clear that demonstrated in this work. Further improvement for long-
f3 > f2 > f1 when the Dchannel-gate increases from 30 to 60 µm and term potentiation may include the large voltage bias adjus-
then to 90 µm, respectively. The capacitance measurements tion or exploring the new solid electrolyte with more charged
can further confirm this point, as shown in Figure S3b (Sup- ions inside. The energy consumption of single spike event can
porting Information). For the frequency is more than ≈1 kHz, be extracted from the equation W = VDS ∫ Ipeak dt, where VDS,
the capacitance does not change significantly. However, at Ipeak, and dt are source–drain voltage, spike peak current, and
the low-frequency domain (<1 kHz), the capacitance decays spike duration time, respectively. As a consequence, the energy
more slowly for Dchannel-gate = 30 µm, compare for Dchannel-gate = consumption of a single spike event can be estimated to be
90 µm. Therefore, a larger Dchannel-gate would result in a lower 23.6 pJ, which is significantly lower than that of the artificial
operational speed in such neuromorphic device. The under- synapse using a conventional CMOS circuit,[10,11] and is com-
lying device physics may be ascribed from the ion migration parable to that of the reported hardware-based artificial syn-
limitation at the low-frequency domain in such a proton-con- apse.[5–7,16,17] Herein, the spike duration-dependent EPSC can
ducting neuromorphic device. also be studied (spike amplitude: 1 V), as shown in Figure 2d.
Figure 2a shows a schematic diagram for a neural net- The amplitudes of the EPSC increase from ≈23.6 to 294 nA for
work in which nodes (neurons) are connected by lines where spike duration time ranging from 10 to 1000 ms, respectively.
the synapses are located at the junctions between adjacent Interestingly, the amplitudes of the EPSC increase almost lin-
neurons. It is evident that every node parallelly processes early within a small spike duration range below 100 ms, while

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Figure 2.  a) Schematic diagram for a neural network in which nodes (neurons) are connected by lines where the junctions between neurons
are corresponding to synapses. b) A magnified schematic diagram for two adjacent neurons with a synapse. c) A typical EPSC of MoS2 synaptic
transistor triggered by a presynaptic spike (1.0 V, 10 ms). d) Spike duration-dependent EPSC, where the spike amplitude: 1.0 V. Inset: fitting EPSC
decay phenomenon by using the exponential decay model. e) A pair of presynaptic spikes and a triggered EPSC are shown versus time. f) A 2D PPF
index surface is summarized as a function of V+ and V−.

it will get saturated when the spike duration is above 100 ms. where A0, A1, τ, and t0 are the final value of decay current, the
This biological response can be simply explained as follows: EPSC amplitude, retention time constant, and the time when
in the beginning, more and more protons will migrate to the the presynaptic spike finished, respectively. Fitting the data to
2D MoS2 channel interface and thus increase the channel Equation (1), the τ is found to be ≈13 ms, which indicates that
conductivity (i.e., synaptic plasticity) of 2D synaptic device.[44] the feature time of proton migration is about 13 ms.
However, there are only limited activated protons in the PVA In a biological system, PPF is a form of short-term syn-
membrane. As a result, the EPSC amplitude would be gradu- aptic plasticity and plays a key role in decoding the tem-
ally saturated with a longer spike duration time. Furthermore, poral information for auditory or visual signals.[2] PPF (i.e.,
as shown in the inset of Figure 2d, such proton-induced EPSC neural facilitation in neuroscience) is a typical phenomenon
decay phenomenon can be well fitted by using the exponential in which EPSC evoked by the spike is increased when the
decay model as the following equation[20] second spike closely follows a previous spike.[2,8,9,58] Such a
typical neuron behavior can also be mimicked in our artificial
 t − t0  2D MoS2 synaptic transistor. Figure 2e shows the EPSC trig-
A ( t ) = A0 + A1 ⋅ exp  −
 τ 
 (1)
gered by a pair of presynaptic spikes with a pulse interval (Δt)

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of 40 ms. Two continuous presynaptic spikes were applied on function of presynaptic voltage of V+ and V− . From this 2D
the presynaptic input (coplanar metal gate) in close suc- surface, the PPF index can be continuously tuned accordingly.
cession: pulse voltage (V+) = 1.5 V, pulse duration = 10 ms, It is clear that a more negative V− and positive V+ result in
and base voltage (V−) = −0.6 V. From this figure, it is clear a larger PPF value. The maximum PPF index is observed to
that the EPSC triggered by the second presynaptic spike be as high as 367 with the V− of −0.9 V and V+ of 1.5 V. Such
(658.3 nA) is much larger than that triggered by the first one a modulated PPF index is very beneficial for neuromorphic
(511.7 nA). When the interval is smaller than the ionic relax- computing in the biological system.
ation time, some of the protons triggered by the first spike Synaptic plasticity is defined as the efficacy variation
could not come back to their equilibrium position. Then the during synaptic transmission.[2,59] Such efficacy variation
channel current is thus facilitated by the EDL modulation of consumes tens of milliseconds which can also be called facili-
the residual protons at the MoS2/PVA interface. Here, the tation or short-term depression. Such neuronal behaviors
PPF index of the 2D MoS2 artificial synapse can be defined are often activated by different temporal events. Thus, short-
A term plasticity would result in a temporal filtering through
as follows: PPF = 2 × 100%, where A1 and A2 are the EPSC
A1 impeding signal transmission or facilitating signal transmis-
peak of the first and second spikes, respectively. As shown in sion for different patterns.[2,59] The inset of Figure 3a shows
Figure 2f, a 2D PPF index surface can be summarized as a a schematic diagram of synaptic filter. In this model, neurons

Figure 3.  a) EPSCs recorded in response to the stimulus train with different frequencies. Inset: a schematic diagram showing the convergence
of depressing and facilitating afferent synapses for the generation of a temporal filtering function. b) EPSC amplitude ratio (A10/A1) plotted as a
function of the presynaptic spike frequency. Inset: a schematic diagram showing artificial MoS2 synapse for the generation of a high-pass temporal
filtering function. c) A schematic diagram for dendritic integration in single dendritic branch. d) A two-layer network model of hierarchical parallel
processing of dendrite. e) EPSCs triggered by two spatiotemporally correlated inputs (1.0 V, 10 ms) with different time intervals of −50, 0, and
50 ms, respectively. The EPSCs triggered by each individual input are also shown in the top of the figure. f) The dynamic logic established by the
two spatiotemporally correlated spikes. The EPSC amplitudes were measured at t = 0.

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receive inputs from two classes of synapses: some exhibits EPSC triggered by spike1. Accordingly, EPSC measured at
strong short-term depression, while others show strong short- zero time is clearly larger than the EPSC triggered only by
term facilitation. Such depression generally occurs at “high- spike1. As a contrast, when the spike2 is triggered later than
Pr” (high probability of release) synapses, whereas short-term spike1 (e.g., Δt = +50 ms), the EPSC measured at zero time
facilitation is more prevalent at “low-Pr” (low probability is equal to the amplitude triggered only by spike1. It is to
of release) synapses.[59] Accordingly, the short-term syn- be noted that the EPSC even gets much larger if the spike1
aptic depression accounts for low-pass temporal filtering, and spike2 arrive at the same time (i.e., Δt = 0 ms). Figure 3f
and short-term synaptic facilitation accounts for high-pass illustrates the summarized dynamic logic established by the
temporal filtering, respectively. Because a shorter Δt results spatiotemporal correlated spikes, which is unsymmetrical
in a larger PPF index, a high-pass filter may be realized in with increasing Δt. If the Δt > 0, the resulted EPSC is equal
our artificial 2D MoS2 synaptic device.[59] Figure 3a shows to the amplitude triggered only by spike1. While if the Δt < 0,
the EPSC responses of our device to the stimulus train, with protons accumulated at the MoS2/PVA interface will drift
different frequencies ranging from 10 to 50 Hz. The stimulus gradually back to their equilibrium position due to the con-
train at each frequency consists of ten successive stimulus centration gradient, and the resulted EPSC will increase
spikes (1 V, 10 ms), and the VDS is biased to be 0.1 V during with decreasing the |Δt|. Therefore, the maximum EPSC of
EPSC measurements. From this figure, it is clear that at low- ≈138 nA could be obtained at Δt = 0. Such a mimicked spa-
frequency spike stimulation the peak value of the EPSC tiotemporal dynamic logic is very meaningful for neuromor-
increases slightly, while at high-frequency stimulation the phic computing or artificial neural network.
peak value increases significantly, which strongly indicates Figure 4a shows a schematic diagram for an artificial
that our artificial 2D MoS2 synaptic transistor can actually act neuron with branched dendrites, where Wi (i = 1,2…n and m)
as a high-pass filter. Here, the frequency-dependent gain can represents each synaptic input weight. Such dendrites can pro-
be defined as the ratio between the tenth EPSC (A10) and cess and integrate many presynaptic inputs and then transmit
the first EPSC (A1), as shown in Figure 3b. Interestingly, the the output signals to other neurons through a so-called
gain increases linearly from ≈3.5 to ≈13.5 when the stimulus axon.[61] Here, a multiple-gate 2D MoS2 synaptic transistor
frequency changes from 10 to 50 Hz. Therefore, the results can be proposed for mimicking the multiple-presynaptic den-
presented here indicate that the 2D MoS2 synaptic transistor dritic integration, as schematically shown in Figure 4b. G1 and
can act as a good dynamic high-pass filter for information G2 represent two presynaptic driving-input terminals, and Gm
transmission, as shown in the inset of Figure 3b. Extracting represents a presynaptic modulatory terminal, respectively.
information concerning fast changes in signal amplitude and Figure 4c shows such a spiking logic response by two presyn-
rejecting that from slow fluctuations, that is, high-pass tem- aptic driving inputs and a modulatory input (0.2 V, 10 ms).
poral filtering, are central to the utility of the jamming avoid- From this figure, the postsynaptic spike current exhibits a
ance response.[59] Such high-pass filter function mimicked maximum value of ≈0.72 µA only when both presynaptic
here is very interesting for computing the direction of motion driving inputs are applied with high spike voltage. Here, if we
of an electric image and therefore directional selectivity in set a threshold line with 0.5 µA of the postsynaptic current
artificial nervous systems.[60] for defining the state “0” and “1” state, “AND” spike logic
As shown in the schematic diagram of Figure 3c, den- could be obtained in such 2D MoS2 synaptic device. As a con-
drites deliver electrical/chemical signals to the soma, but they trast, the postsynaptic spike current increases to be ≈1.29 µA
are not just simple conductors of information.[60,61] Dendritic when both presynaptic driving inputs are applied with high
integration can be performed in single dendritic branch, spike voltage and a higher modulatory input (1.5 V, 10 ms)
which plays an important role in information transformation is applied simultaneously, as shown in Figure 4d. Interest-
including addition of nonsimultaneous unitary events (tem- ingly, the postsynaptic spike current increases nonlinearly to
poral summation) and addition of unitary events occurring be above the threshold line when only a single presynaptic
simultaneously in different regions of the dendrite (spatial input is applied with a high spiking voltage, which means
summation).[60,61] Figure 3d exhibits a two-layer network that the spiking logic operation changes from “AND” logic
model with hierarchical parallel processing of dendrite. Pre- to “OR” logic eventually. Figure 4e further summarizes the
synaptic signals can be integrated locally within dendritic sub- truth tables with different modulatory spike inputs of 0.2 and
units, which nonlinearly computes the sum of its local inputs. 1.5 V, respectively. From these tables, it is clear that “AND”
Dendritic spikes are regenerative potentials initiated locally logic and “OR” logic operation can be easily modulated
in dendritic branches when input is sufficiently clustered depending on the third modulatory spiking voltage. At the
in space and time. Such spikes, which are relatively ubiqui- same time, if the measured amplitude of EPSC (Isum, both
tous across different cell types, can be effectively integrated presynaptic spikes are in high voltage level) is plotted as
depended on a threshold for the local spatiotemporally dis- a function of the arithmetic EPSC sum (I1 + I2, only single
tributed inputs.[61] Here, two spatiotemporally correlated presynaptic spike is in high voltage level), Figure 4f can sys-
stimuli of dendritic spikes (1 V, 10 ms) can be used to mimic tematically summarize the results with different modula-
the spatiotemporal dynamic logic in such a 2D MoS2 synapse tory spiking voltages. It is clear that the amplitudes of EPSC
transistor, as shown in Figure 3e. First, the time of spike1 is can be effectively modulated by the spike applied on Gm.
defined as t = 0 ms. When the spike2 is triggered earlier than For example, when a spike (1.4 V, 10 ms) is applied on Gm,
spike1 (e.g., earlier with 50 ms, i.e., Δt = −50 ms), the residual a linear synaptic integration behavior is observed. How-
protons triggered by spike2 can enhance the following ever, a sublinear synaptic integration is observed when the

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Figure 4.  a) A schematic diagram of an artificial neuron with branched dendrites, where Wi (i = 1, 2…n and m) represents the synaptic weight of
each input. b) A schematic diagram of multiple-gate MoS2 neuromorphic transistor. c) A spiking logic response by two presynaptic driving inputs
and a modulatory input (0.2 V, 10 ms). d) A spiking logic response by two presynaptic driving inputs and a modulatory input (1.5 V, 10 ms). e) The
truth tables for “AND” logic for Vm = 0.2 V and “OR” logic for Vm = 1.5 V, respectively. f) The measured sum plotted as a function of expected sum.

amplitude of Vm is increased to 1.5 V. These results indicate the slope (gain) and offset of such relationships represent
that the superlinear and sublinear synaptic integration could defined mathematical operations.[63,64] As shown in Figure 5a,
be realized through modifying the spiking voltage of the the slope change denotes the multiplicative operation,
modulatory terminal. Such results are of great significance R(x, m) = F(x) × G(m), while the offset (intercept) change
for synaptic electronics and neuromorphic computing. denotes the additive operation, R(x, m) = F(x) + G(m).
On top of this, neural coding and gain modulation can Figure 5b schematically shows the rate coding diagram where
be demonstrated in such multiple-gate MoS2 neuromorphic the information is encoded by the rate (f = f1 + f2) of driving
device. A neuron with branched dendrites can process and inputs. Herein, the driving input parameter in our artifi-
integrate many presynaptic inputs and then transmit the cial 2D neuromorphic device can be defined by the rate of
output signals to other neurons through a so-called axon.[5] driving input (i.e., x = f), and the modulatory input para­meter
Understanding how neurons process the rate-coded infor- is defined by the modulatory voltage (m = Vm), and thus
mation is of great significance in the neural computation of the EPSC amplitude is regarded as the output parameter
the human brain.[2,62] Such rate-coded neuronal process can in the device output terminal. Figure 5c presents the typical
be expressed from the relationship between mean input and responses (Vm = 0) to the spike trains with driving inputs
output firing rates (i.e., I–O relationship).[63,64] Changes in (0.5 V, 10 ms) of a rate of 40 and 100 spikes s−1, respectively.

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Figure 5.  a) A schematic figure of neural coding with multiplicative operation and additive operation, respectively. b) The schematic diagram
of the rate coding scheme in a neuron with two driving synapses and a modulatory synapse. c) The typical EPSC responses (Vm = 0 V) with two
driving spike inputs (0.5 V, 10 ms) with a rate of 40 and 100 spikes s−1, respectively. d) The neuronal I–O relationships with rate coding scheme
modulated by different modulatory voltages of 0, −0.2, and −0.4 V, respectively. Solid lines are the linear fitting results by using the equation
y = kx + b. e) The summarized slopes and x-axis intercepts as a function of Vm through the linear fitting from neuronal I–O relationships. f) Adding
excitation shifts the curve to the left, and inhibition shifts it to the right. Neural gain modulation corresponds to a tipping of the I–O curve, which
results in a change of its slope.

Here, the mean EPSC amplitude (A) can be defined as the This linear fitting to the I–O relationship can be imple-
resulted output during neuronal spike response. Accordingly, mented by using the equation y = kx + b, where the x-axis
the resulted A can be extracted to be 0.22 and 0.48 µA for the intercept can be extracted as xo = − b/k. Figure 5e shows the
input spike rate of 40 and 100 spikes s−1, respectively. Figure 5d slope (k) and x-axis intercept (xo) of the linear fitting as a
shows the output A as a function of input spike rate ranging function of Vm. The xo is tuned from −4.46 to −0.825 and then
from 10 to 100 spikes s−1 with different Vm of 0, −0.2, and to 5.67 spikes s−1 when the Vm changed from 0 to −0.2 and
−0.4 V, respectively. Interestingly, the output A increased with then to −0.4 V, respectively. This indicates that an additive
increasing the input spike rate by a linear manner. What’s mathematical operation (more specifically, a subtractive
more, the EPSC output would be decreased a lot when a neg- manner) has been realized by decreasing the Vm. At the same
ative Vm is applied, which means that an effective neuronal time, more importantly, the slope value sharply decreases
output modulation could be realized by this way.[63] from 4.85 to 3.61 and then to 1.77 nAs/spikes when the Vm is
Furthermore, a good linear fitting can be performed for modulated from 0 to −0.2 and then to −0.4 V, respectively. As
the I–O relationship as shown in the solid line of Figure 5d. shown in Figure 5f, slope change represents the multiplicative

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operation (i.e., neuronal gain modulation), while the x-axis neuromorphic devices were measured by a semiconductor para­
intercept change represents the additive operation (adding meter characterization system (Keithley 4200 SCS) under a relative
excitation shifts the curve to the left, and inhibition shifts it humidity of ≈50% at room temperature. Presynaptic spikes were
to the right).[65,66] As a result, neuronal gain modulation has applied on the coplanar lateral gate electrodes, and postsynaptic
been successfully implemented through the control of modu- current output was measured by applying a small reading voltage
latory presynaptic input in our multiple-gate 2D MoS2 neuro- between the source and drain electrode.
morphic device. Neuronal gain control is of great importance
for processing information in the human brain.[65,66] The
nonlinear multiplicative operation is fundamental to coordi-
nate transformations for object perception and for all kinds
of spatial processing, from eye-hand coordination to naviga- Supporting Information
tion.[65,66] Therefore, such artificial 2D MoS2 neuromorphic
device could be possibly applied in the intelligent neuronal Supporting Information is available from the Wiley Online Library
computing and complex object recognition applications for or from the author.
future advanced nanoelectronics, which is very hard to be
completed using the traditional approach.
In summary, multigate 2D MoS2 neuromorphic devices Acknowledgements
laterally coupled by proton-conducting PVA electrolytes
were fabricated. The coplanar lateral metal gates and 2D This work was supported by the National Natural Science Foundation
multilayer MoS2 can be regarded as presynapse and post- of China (Grant Nos. 61404176 and 11334014), National Science
synapse, respectively. Multiple presynaptic inputs can be Foundation for Distinguished Young Scholars of China (Grant
spatiotemporally coupled in such 2D MoS2 neuromor- No. 61425020), the Open-End Fund for the Valuable and Precision
phic transistor. EPSC, PPF, dynamic filter, spatiotemporal Instruments of Central South University, and the Opening Project of
signal dendritic integration, and spike logic realization and Key Laboratory of Microelectronic Devices & Integrated Technology,
modulation were successfully emulated. Most importantly, Institute of Microelectronics, Chinese Academy of Sciences.
multiplicative neural coding and neuronal gain modulation
were also experimentally demonstrated. Such artificial 2D
MoS2 neuromorphic devices are of great significance for real- Conflict of Interest
izing the intriguing artificial intelligence in 2D nanoscale neu-
romorphic cognitive systems, such as directional selectivity, The authors declare no conflict of interest.
object recognition, sensory processing, etc.

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