Artificial Synapses with Short- and Long-Term Memory for Spiking

Aug 24, 2017 - (29) In addition, biopolymers have advantages, such as simple fabrication process and flexibility, which facilitate their application f...
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Artificial Synapses with Short- and Long-Term Memory for Spiking Neural Networks Based on Renewable Materials Youngjun Park and Jang-Sik Lee* Department of Materials Science and Engineering, Pohang University of Science and Technology (POSTECH), Pohang 790-784, Republic of Korea S Supporting Information *

ABSTRACT: Emulation of biological synapses that perform memory and learning functions is an essential step toward realization of bioinspired neuromorphic systems. Artificial synaptic devices have been developed based mostly on inorganic materials and conventional semiconductor device fabrication processes. Here, we propose flexible biomemristor devices based on lignin by a simple solution process. Lignin is one of the most abundant organic polymers on Earth and is biocompatible, biodegradable, as well as environmentally benign. This memristor emulates several essential synaptic behaviors, including analog memory switching, short-term plasticity, long-term plasticity, spike-rate-dependent plasticity, and short-term to long-term transition. A flexible lignin-based artificial synapse device can be operated without noticeable degradation under mechanical bending test. These results suggest lignin can be a promising key component for artificial synapses and flexible electronic devices. KEYWORDS: biopolymers, lignin, memristors, artificial synapses, flexible electronics

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To achieve highly efficient artificial synapses, various types of devices have been considered, such as phase changes, ferroelectrics, and memristor-based synapses.3,12−15 The memristor is an attractive structure for artificial synapses because it has two-terminal structure that is analogous to biological synapse, and applied electrical bias can affect its resistance.16−19 Memristors also have advantages of scalability, fast operation, and applicability as three-dimensional structure.20−22 Furthermore, the structures have a potential to be packed at higher density and to have lower power consumption than conventional CMOS implementations.15,23 However, most memristors have been based on inorganic materials that are fragile and incompatible with flexible and versatile

euromorphic computing is a promising concept as a new computing system that is highly efficient, consumes little energy, is fault-tolerant, and may overcome the limitations of conventional von Neumann architecture.1,2 Neuromorphic computing structure emulates a human brain that concurrently performs perception, learning, and memory. These functions are performed by enormous numbers of neurons (∼1012) and synapses (∼1015). In particular, the synapses perform learning and memory functions by modulating the strength of connection between neurons; this process is called synaptic plasticity.3 Therefore, emulation of a synapse is an important step to achieve an efficient artificial neuromorphic system. Recently, devices with single artificial synapse based on complementary metal-oxide semiconductor (CMOS) analogue circuits with several transistors and capacitors were fabricated, but complex integrated circuits were required with high power consumption.4,5 Thus, new materials, structures, and devices have been evaluated.6−11 © 2017 American Chemical Society

Received: May 14, 2017 Accepted: August 24, 2017 Published: August 24, 2017 8962

DOI: 10.1021/acsnano.7b03347 ACS Nano 2017, 11, 8962−8969

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Figure 1. (a) Lignin, one of main components of plants. (b) Schematics of Au/lignin/ITO/PET artificial synapse device. (c) Image of the flexible artificial synapse device. (d) Chemical structure of lignin.

Figure 2. Nonlinear responses of lignin-based synaptic device. (a) I−V characteristics of the device during 5 consecutive positive and negative sweeps. (b) Changes of device conductance during consecutive sweeps. (c) Current responses with time according to applied bias pulses. (d) Variation of current after 50 consecutive negative pulses (−0.7 V, 100 ms), then 50 consecutive positive pulses (+0.7 V, 100 ms).

functionality.24,25 In addition, these materials lack biocompatibility and biodegradability, which are required for implantable applications. For such applications, new materials should be developed. Biopolymers have been considered as replacements for rigid silicon-based materials in electronic devices.26−28 Biopolymers do not require complex chemical synthesis and assembly that cause environmental problems and consume large amounts of energy.29 In addition, biopolymers have advantages, such as simple fabrication process and flexibility, which facilitate their application for wearable, flexible, and implantable devices.30,31 We suggest use of lignin for an artificial synaptic device. Lignin is an organic component of woods and is a random and

three-dimensional network polymer composed of complex aromatic structures.32 Lignin is a very abundant natural material on Earth and is a waste product of the pulp-and-paper industry.33,34 This study suggests use of lignin-based memristors as artificial synapses for the following reasons. First, lignin has high carbon contents compared to other polymers;35 heat can transform it into amorphous or graphitic structures and may thereby change its electrical conductivity;32 this property can be exploited for use in an artificial synapse in which the properties can change in response to the electrical signals applied to it. Second, use of lignin can reduce the cost of device fabrication. To mimic the human brain, many synapse devices are required, so the reduction of production cost will be 8963

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Figure 3. (a) Profile of one cycle of applied bias pulse. (b) Measured currents for 10 pulse cycles with different pulse intervals. (c) Mean changes ΔI of current during cycles of 10 pulses at different intervals (error bars: standard deviation from measurement of 10 devices). (d) Mean ΔI after consecutive pulses (ΔI = I2 − I1) and after the tenth pulse (ΔI = I10 − I1), which indicate PPF and PTP, respectively (error bars: standard deviation from measurement of 10 devices).

Typical current−voltage (I−V) characteristics of lignin-based device were demonstrated by applying direct current (DC) voltage to the Au top electrode while the ITO bottom electrode was electrically grounded (Figure 2a). The applied voltage was carefully controlled to avoid abrupt binary resistive switching behavior, that is, abrupt change in resistance state from high to low.39 When 5 consecutive sweeps of negative DC voltages from 0 to −0.7 V were applied to the device, the current level increased after each sweep; this response is similar to synaptic potentiation of biological synapses. Then when 5 consecutive sweeps of the opposite polarity (0 to +0.7 V) were applied to the device, the current level decreased after each sweep. The conductance at 0.1 V increased or decreased gradually over 10 consecutive sweeps (Figure 2b). To more clearly demonstrate the change by consecutive sweeps, current responses with time according to applied bias pulses were measured (Figure 2c). These gradual changes in conductance emulate a successively variable synaptic weight, that is, variable connection strength. The conductance can be also modulated by continually applying a programmed pulse. Fifty consecutive identical negative pulses (−0.7 V, 100 ms) were applied to potentiate the conductance in the device, and then 50 consecutive positive pulses (+0.7 V, 100 ms) were applied to depress it. A small read pulse with an amplitude of 0.1 V, which does not influence the device operation, was applied after each consecutive pulse (Figure 2d). These results showed that conductance was also gradually potentiated or depressed by the consecutive pulses. To test whether film thickness affected the switching behavior, we fabricated lignin-based devices with films of different thickness by controlling the spin speeds during spin-coating. The lignin film layer was deposited at spin-coating speeds of 800, 1000 (Figure S2), and 1200 rpm (Figure 2a). When consecutive sweeps were applied, analog switching behaviors were observed in all cases, but with slightly changed current levels due to different thicknesses (Figure S2).

very important to reduce the overall cost of synapse devices. Lignin is very inexpensive due to its abundance, accessibility in nature, and its status as a waste product of the pulp industry. Also, thin films of lignin can be easily synthesized using the solution process.36,37 Therefore, lignin is very appropriate for a low-cost process. Third, this material is useful for biocompatible and implantable applications because it is nontoxic, ecologically benign, and biodegradable.35,38 In this study, we fabricated and characterized an artificial synapse device that is based on lignin, a natural polymer. The lignin layer was deposited by solution process at room temperature. The as-fabricated device showed essential functions as a single artificial synapse, including potentiation and depression, spike-rate-dependent plasticity (SRDP), and short-term to long-term transition, all of which were comparable to those of inorganic devices. Also, we confirmed that the device operates while being flexed. These results demonstrate the feasibility of biopolymer-based artificial synapses for neuromorphic systems.

RESULTS AND DISCUSSION A two-terminal artificial synapse device was fabricated on indium tin oxide (ITO)-coated flexible polyethylene terephthalate (PET) to emulate a biological synapse (Figure 1). Lignin was deposited by spin-coating at a spin-coating speed of 1200 rpm for use as an active layer in the artificial synapse (cross-sectional scanning electron microscopy (SEM) image of lignin can be found in Figure S1). To minimize the effect of metal ions on the function of the device, Au (an inert metal) was used as the top electrode. The Au top electrode emulates presynaptic neurons, and the ITO bottom electrode emulates postsynaptic neurons. Electrical pulses that represent synaptic spikes were applied to induce synaptic behaviors in the asfabricated device. 8964

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after stimulation. The postsynaptic current increased abruptly and then decayed gradually over time (Figure 4).

To confirm the applicability of this artificial synapse as a flexible device, we measured its electrical characteristics during bending (Figure S3). Consecutive DC voltage sweeps were applied in the same way as measurement in the flat state. Although the current levels changed somewhat, analog switching behaviors were also observed in the bent state; these results showed the possibility of application as flexible devices. Ideally, the electrical properties should not change under different bent conditions. We are performing studies to optimize device fabrication parameters to improve the uniformity of electrical properties. We measured the effect of temperature on the artificial synapse behaviors before and after 5 consecutive negative sweeps (Figure S4). Conductance was measured at 0.1 V. When temperature increased from 20 to 100 °C, the resistance state was maintained without noticeable degradation. This result shows that this lignin-based artificial synapse can be operated at least up to 100 °C. Reaction with moisture in air can be avoided by depositing a passivation layer. Al2O3 thin film was deposited on fabricated lignin-based synapse by using atomic layer deposition (ALD). Five consecutive negative sweeps from 0 to −0.7 V were applied, and conductance was measured at 0.1 V. The device operated without noticeable degradation for 11 days (Figure S5). Simple passivation process using thin oxide layer can extend the lifetime of the device. In neuromorphic systems, synaptic plasticity is regarded as learning and memory function by adjusting a synaptic weight.3 One basic characteristic of synaptic plasticity is spike-ratedependent plasticity (SRDP).40−43 To investigate the effect of the spiking rate, we applied pairs of consecutive stimulus pulses separated by different intervals. Each stimulation cycle was composed of one stimulation pulse (−0.7 V, 100 ms) and one read pulse (0.1 V, 100 ms) (Figure 3a). Stimulation at 100 ms intervals caused increase in current, whereas stimulation at 10 s intervals caused negligible change in current (Figure 3b). Current changed further as the interval between pulses decreased (Figure 3c). In a biological synapse, stimulation of the presynapse by an action potential (spike) induces influx of Ca2+ ions, which stimulate release of neurotransmitters; the process temporarily amplifies synaptic transmission. The concentration of Ca2+ ions requires time to recover to its original state, so if a second identical stimulation is applied before complete recovery, the postsynapse response after the second stimulation is larger than the first one; this effect is called paired-pulse facilitation (PPF).44,45 As a consequence of this reaction, synaptic transmission gradually increases if many sequential stimulations are applied in short time; this effect is called post-tetanic potentiation (PTP).46 To evaluate whether the artificial synapse demonstrates analogous behaviors, we compared the change in current after the second pulse (I2 − I1) and after the tenth consecutive pulse (I10 − I1); these changes correspond to PPF and PTP, respectively (Figure 3d). Both comparisons demonstrate that the synaptic response in the lignin-based artificial synapse increased when sequential pulses were applied with the appropriate spike rate, and that the synaptic weight can be adjusted by controlling the spike rate. The change in conductance after consecutive pulses is attributed to the temporal interaction between applied stimulation (spike) and the ionic excitatory postsynaptic current (EPSC).47 To measure EPSC, an electrical pulse (−0.7 V, 10 ms) was used as the stimulus and a voltage bias (0.1 V) was applied continually to read the current changes

Figure 4. EPSC characteristic with voltage pulse stimulation (−0.7 V, 10 ms).

Generally, synaptic plasticity can be divided into short-term plasticity (STP) and long-term plasticity (LTP), depending on retention time.48−50 Both phenomena describe a change in synaptic weight: in STP, the change is a temporal change of synaptic weight that lasts only a few seconds; in LTP, the change can be maintained for a relatively long time. STP can be transformed to LTP by repeated rehearsal events.46 To measure the transition, different number of pulses (10 ≤ N ≤ 50) as stimuli were applied to the presynapse, with other conditions of the applied pulse fixed. Continuous voltage bias (0.1 V) was applied to read the current level changes. The normalized synaptic weight decreased rapidly in the initial stage but then decreased slowly over time and finally reached an intermediate level (Figure 5a−e). To explain the transition, the normalized current It at a given time t was fitted using a modified Kohlrausch equation, which is frequently used as forgetting function in psychology:51 It = I0 + A exp( −t /τ )

(1)

where I0 is the current in the stabilized state, A is a prefactor, and τ is a relaxation constant, which implies forgetting rate. As the number of applied stimulation pulses increased, relaxation time increased (Figure 5f). These results show the feasibility of transition from STP to LTP in the lignin-based artificial synapse. We emulated learning, forgetting, and relearning processes using lignin-based synapse devices. First, 50 consecutive negative pulses were applied, while the change of synaptic weight was measured at 0.1 V (Figure 6a). Then, spontaneous decay of synaptic weight was observed with time (Figure 6b). Finally, 20 consecutive bias pulses were applied after the spontaneous decay (Figure 6c). It is interesting to note that 20 pulses were enough to obtain the same synaptic weight before spontaneous decay occurred. This phenomenon is similar to relearning in the brain, which relearns forgotten information more quickly than for the first time.42,47 We also plotted the figures with conductance levels (Figure S6). To analyze the synaptic behavior of the lignin-based device, the transport mechanism of charge carriers was analyzed. A log−log plot of the I−V characteristic during the first sweep is divided into two distinguishable slopes (Figure S7). Ohmic conduction (I ∼ V) with a slope of 1 was exhibited in the low voltage region because thermally generated carriers were more abundant than injected carriers. Quadratic behavior (I ∼ V2) occurred at high voltage region; this trend implies that injected carriers were dominant for conduction because sufficient electric field was applied to fill the trap center.52,53 On the 8965

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Figure 5. Short-term to long-term transition. (a−e) Changes of synaptic weights and fitted curves after different number (N) of applied pulses (N = 10, 20, 30, 40, and 50). (f) Changes of relaxation time with each pulse cycle. Inset in (a) shows applied pulses and reading bias.

Figure 6. Learning experience of the lignin-based device. (a) Increase of synaptic weight with 50 consecutive pulses. (b) Spontaneous decay of synaptic weight with time. (c) Increase of synaptic weight with consecutive 20 pulses.

In a lignin-based artificial synapse, device operation may be related to the behavior of carbon atoms in the lignin active layer. By applying thermal energy, the lignin can be carbonized and transformed to an amorphous carbon matrix or to graphitic structures, and this change can affect conductance.32 When electrical bias is applied to the device, the weakest points break down as a result of Joule heating. A large bias can facilitate local breakdown that induces pyrolysis, which generates localized carbon-rich regions that may be converted to amorphous carbon.53,56,58 As the heat applied increases, the amorphous carbon can be converted to localized graphitic structures; this process induces change of conductance.59−61 However, in this study, we controlled the applied bias to avoid binary resistive

contrary, Ohmic conduction was observed during voltage sweep back to 0 V; this linear I−V characteristic (slope of ∼1) indicates that conductive filaments formed when negative DC bias was applied.53,54 The filamentary conduction mechanism in organic-based devices has been attributed to development of metallic paths by diffusion of electrode materials or to development of carbon-rich filament due to degradation of organic thin film.55−57 Thus, we measured the lignin-based device with different electrodes to confirm the effect of electrode materials on switching behaviors. Al was used as the top electrode, and analog switching behavior was also observed (Figure S8); this result indicates that analog switching behavior is not thought to be related to electrode materials. 8966

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ACS Nano switching behavior that shows abrupt resistance change.62 The applied electrical bias does not supply sufficient heat to drive formation of a stable conductive filament,25 so the unstable filament that forms can be easily ruptured by Joule heating or by mechanical stress induced by the electrical field.63 If brief pulses with low amplitude are applied, an unstable filament forms, but the unstable filament may be easily broken; this trait underlies the mechanism of STP. If the applied number of pulses is increased, the formed filament can be changed. Applied pulses facilitate Joule heating; this resulting heat drives formation of stable filaments. Although some unstable filaments may be broken, the stable filaments remain; as a result, repeated pulses cause in change of conductance, and when the pulses are withdrawn, it does not decay fully to its initial state. Therefore, when short number of pulses are applied, EPSC behavior occurs due to the instability of the unstable conductive filaments, but conductance was maintained at the intermediate state for a long time when large number of pulses are applied. These characteristics emulate short-term to long-term transition in biological synapses.

ASSOCIATED CONTENT S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.7b03347. SEM image of lignin layer, I−V characteristics with different thicknesses and electrodes, mechanical flexibility under bent state, temperature and long-term stability, learning experience of synapse plotted with conductance level, double logarithmic plot of lignin-based synapse in Figures S1−S8 (PDF)

AUTHOR INFORMATION Corresponding Author

*E-mail: [email protected]. ORCID

Jang-Sik Lee: 0000-0002-1096-1783 Author Contributions

J.-S.L. conceived and directed the research. J.-S.L. and Y.P. designed and planned the experiment. Y.P. performed the experiment and acquired the data. Y.P. and J.-S.L. wrote the manuscript.

CONCLUSIONS

Notes

We fabricated lignin-based artificial synaptic devices that have analog switching properties. The devices showed gradual changes in conductance when consecutive voltage pulses were applied. The devices were also operated stably while being bent. In addition, the lignin-based artificial synapse successfully emulated fundamental synaptic functions including potentiation/depression, EPSC, SRDP, and transition from STP to LTP. Our research presents methods that use natural, inexpensive, and environmentally benign biopolymers to develop artificial synapses for neuromorphic systems. Also, these results suggest that lignin can be considered as a key component for biocompatible and implantable artificial synapses in the future.

The authors declare no competing financial interest.

ACKNOWLEDGMENTS This work was supported by National Research Foundation of Korea (NRF-2016M3D1A1027663, NRF2015R1A2A1A15055918). This work was also supported by Future Semiconductor Device Technology Development Program (10045226) funded by the Ministry of Trade, Industry & Energy (MOTIE)/Korea Semiconductor Research Consortium (KSRC). In addition, this work was partially supported by Brain Korea 21 PLUS project (Center for Creative Industrial Materials). REFERENCES (1) Jeong, D. S.; Kim, K. M.; Kim, S.; Choi, B. J.; Hwang, C. S. Memristors for Energy-Efficient New Computing Paradigms. Adv. Electron. Mater. 2016, 2, 1600090. (2) Jo, S. H.; Chang, T.; Ebong, I.; Bhadviya, B. B.; Mazumder, P.; Lu, W. Nanoscale Memristor Device as Synapse in Neuromorphic Systems. Nano Lett. 2010, 10, 1297−1301. (3) Kuzum, D.; Yu, S.; Philip Wong, H.-S. Synaptic Electronics: Materials, Devices and Applications. Nanotechnology 2013, 24, 382001. (4) Diorio, C.; Hasler, P.; Minch, A.; Mead, C. A. A Single-Transistor Silicon Synapse. IEEE Trans. Electron Devices 1996, 43, 1972−1980. (5) Hahnloser, R. H. R.; Sarpeshkar, R.; Mahowald, M. A.; Douglas, R. J.; Seung, H. S. Digital Selection and Analogue Amplification Coexist in a Cortex-Inspired Silicon Circuit. Nature 2000, 405, 947− 951. (6) Zhu, L. Q.; Wan, C. J.; Guo, L. Q.; Shi, Y.; Wan, Q. Artificial Synapse Network on Inorganic Proton Conductor for Neuromorphic Systems. Nat. Commun. 2014, 5, 3158. (7) Yu, S. M.; Gao, B.; Fang, Z.; Yu, H. Y.; Kang, J. F.; Wong, H. S. P. A Low Energy Oxide-Based Electronic Synaptic Device for Neuromorphic Visual Systems with Tolerance to Device Variation. Adv. Mater. 2013, 25, 1774−1779. (8) Lee, M. S.; Lee, J. W.; Kim, C. H.; Park, B. G.; Lee, J. H. Implementation of Short-Term Plasticity and Long-Term Potentiation in a Synapse Using Si-Based Type of Charge-Trap Memory. IEEE Trans. Electron Devices 2015, 62, 569−573. (9) van de Burgt, Y.; Lubberman, E.; Fuller, E. J.; Keene, S. T.; Faria, G. C.; Agarwal, S.; Marinella, M. J.; Alec Talin, A.; Salleo, A. A Non-

METHODS Device Fabrication. Low sulfonate alkali lignin powder was purchased from Sigma-Aldrich and dissolved in 1 M NH4OH solution in distilled water (10 mL) to obtain 1 wt % lignin solution. The prepared lignin solution was mixed overnight under constant stirring at 200 rpm and room temperature. To fabricate flexible artificial synapse, the indium−tin−oxide (ITO)-coated polyethylene terephthalate (PET) was used as the flexible substrate. The flexible substrate was sequentially ultrasonicated in acetone, isopropyl alcohol, and distilled water to remove impurities for 15 min each and then blown dry with nitrogen. The cleaned substrate was treated with UV ozone. The lignin solution was spin-coated on the flexible substrate at 500 rpm for 5 s, then 800, 1000, or 1200 rpm for 60 s each. The obtained layers were dried for 48 h to remove the residual solvents at room temperature. The 100 nm thick Au was deposited using the thermal evaporator at 6 × 10−6 Torr. A dot-shaped Au was used as the top electrode through a shadow mask with 100 μm diameter. Al2O3 thin film was deposited at 70 °C using ALD to passivate lignin-based artificial synapses. Characterization. Cross-sectional images of the deposited active layers were observed using a field-emission SEM (JSM 7800F, JEOL). The electrical characteristics of lignin-based synapse devices were measured using a semiconductor parameter analyzer (4200SCS, Keithley) in the probe station. During measurement, the bottom electrode was grounded, and DC voltage sweep was applied to the top electrode. 8967

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DOI: 10.1021/acsnano.7b03347 ACS Nano 2017, 11, 8962−8969