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Synaptic Iontronic Devices for Brain-Mimicking Functions: Fundamentals and Applications ∥ ∥ Changwei Li, Tianyi Xiong, Ping Yu,* Junjie Fei,* and Lanqun Mao

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www.acsabm.org Review Synaptic Iontronic Devices for Brain-Mimicking Functions: Fundamentals and Applications ∥ ∥ Changwei Li, Tianyi Xiong, Ping Yu,* Junjie Fei,* and Lanqun Mao Cite This: ACS Appl. Bio Mater. 2021, 4, 71−84 Read Online ACCESS Metrics & More Article Recommendations ABSTRACT: Inspired by the information transmission mechanism in the central nervous systems of life, synapse-mimicking devices have been designed and fabricated for the purpose of breaking the bottleneck of von Neumann architecture and realizing the construction of effective hardware-based artificial intelligence. In this case, synaptic iontronic devices, dealing with current information with ions instead of electrons, have attracted enormous scientific interests owing to their unique characteristics provided by ions, such as the designability of charge carriers and the diversity of chemical regulation. Herein, the basic conception, working mechanism, performance metrics, and advanced applications of synaptic iontronic devices based on three-terminal transistors and two-terminal memristors are systematically reviewed and comprehensively discussed. This Review provides a prospect on how to realize artificial synaptic functions based on the regulation of ions and raises a series of further challenges unsolved in this area. KEYWORDS: iontronics, memristor, transistor, artificial synapse, neuromorphic device 1. INTRODUCTION numerous regulation strategies including charge transport,21 22 ff Inspired by the synapse structure in the nervous system noncovalent interactions, and so on. (3) The di erent carrying almost all intelligent characteristics of life in a tiny structure of ions provided them diversity in valencies, sizes, 1 and polarizabilities, and as a result, ion current carries more volume with low energy consumption, research attention has 23 been paid to the fabrication of synapse-mimicking devices for information when compared with electronic current. In this artificial intelligence at the hardware level in order to meet the case, iontronics, a newly emerging interdisciplinary conception requirement of diverse neuromorphic computing tasks such as focusing on the designation of devices based on various 24,25 pattern classification,2 decision making, autonomous driving, behaviors of ions, came into sight for the fabrication of and personal healthcare.3 Hitherto, a variety of synaptic synaptic devices including two-terminal memristors and three- devices based on multifarious materials including carbon terminal transistors in the past decade, and synaptic iontronic − Downloaded via UNIV OF NEW SOUTH WALES on April 19, 2021 at 23:18:54 (UTC). materials,4 6 silicon materials,7,8 perovskite structures,9,10 devices, which simulated the synaptic characteristics with ions, ferromagnetic materials,11,12 and metal oxides13 have been were designed and fabricated based on ion doping/transport/ See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. − designed and fabricated since the discovery of transistors in redox in gels,26,27 polymers,28 30 ionic liquids,31 confined Bell Laboratories14 and the development of memristors by HP space,32 and so on. 15 Laboratories. The fabrication of these devices provided a To date, development of synaptic devices, especially synaptic new possibility to the designation of integrated circuits and iontronic devices, has been reviewed in previous reports from raised the efficiency of machine learning. different views. For example, Kuzum et al. systematically sorted ff The main di erence between traditional synaptic devices synaptic devices through the differences in materials, and biological synapses is the species of charge carriers: mechanisms, and applications.33 Yang et al. summarized electrons and holes play the vital role in the conduction of memristive devices for computing,16 and He et al. reviewed electronic synaptic devices, while information was mainly ionic-transistor-based synaptic devices.34 Yu et al. concluded transported and processed based on ions in biological synapses.16 Recent attempts have revealed that ions bear omnifarious unique characteristics providing them great Special Issue: Wearable and Biodegradable Sensors potential for application in the designation of synaptic devices: Received: June 30, 2020 (1) The mobility of ions is much lower than that of electrons, Accepted: August 17, 2020 providing them a potential response ability against external Published: August 17, 2020 stimulation such as light,17 temperature,18 and pressure.19,20 (2) Abundant chemical characteristics of ions contributed to © 2020 American Chemical Society https://dx.doi.org/10.1021/acsabm.0c00806 71 ACS Appl. Bio Mater. 2021, 4, 71−84 ACS Applied Bio Materials www.acsabm.org Review Figure 1. Signal procession in biological synapses and synaptic iontronic devices. (a) Schematic illustration of information transmission in biological (left) and synaptic iontronic devices of different mechanisms (right). Adapted with permission from ref 38. Copyright 2018 WILEY- VCH. (b−d) Synaptic weight changes in synaptic iontronic devices induced by (b) one single spike stimulation and (c) two continuous spike stimulation mimicking paired-pulse facilitation (PPF) in biological synapses (Reprinted with permission from ref 47. Copyright 2015 WILEY- VCH.) and (d) stimulation of continuous spike series mimicking STP−LTP transition. Reproduced from ref 48. Copyright 2012 American Chemical Society. synaptic iontronic devices from structures,35 and Zhu et al. was further demonstrated based on the understanding of reviewed the progress of nanoionic resistive-switching synaptic plasticity in this section. devices.36 However, to the best of our knowledge, little 2.1. Synaptic Plasticity in Biological Synapses and attention has been paid on how ions in synaptic iontronic Synaptic Iontronic Devices. The biological synapse is the devices work and how to regulate ions in these devices, which key junction for signal procession in neural networks. In neural is not only of great importance for the fabrication of iontronic systems, two ways of signaling between synapses formed the devices but also for understanding the characteristics of ions widely connected neural network: ion−ion in electrical fundamentally. synapses and ion−neurotransmitter−ion in chemical synapses. This review systematically summarized the recent progresses Most electrical synapses show simple synaptic behaviors, on of synaptic iontronic devices and was organized into six account of being founded in invertebrates such as fish and sections: The first section briefly introduced the recent crustaceans.37 And the ion−neurotransmitter−ion pathway in progresses in the designation of synaptic iontronic devices. chemical synapses contributed to complex neural functions in The second section focused on the synaptic characteristics higher beings like humans. In this case, understanding and mimicked by the synaptic iontronic devices. The third section mimicking the working mechanism of chemical synapses is of discussed the synaptic iontronic devices based on three great importance for the implantation of synaptic iontronic ff di erent mechanisms, how these devices mimicked the devices. Fundamentally, there are three major components in behaviors of synapses, and how ions contributed to these chemical synapses: presynaptic neuron, synaptic cleft, and mechanisms. The fourth section sorted the evaluation 38 fi postsynaptic neuron (Figure 1a, left panel). In a synaptic standards of the synaptic iontronic devices. The fth section event, ion current signal transmits from the presynaptic neuron introduced the research approach and advanced applications of and drives the release of neurotransmitters to the cleft, further these devices. Finally, a brief summary and the perspective on stimulating the postsynaptic neuron and leading to the this area were presented in the last section. transmission of signal from the presynaptic neuron to the postsynaptic neuron. 2. SYNAPTIC CHARACTERISTICS IN SYNAPTIC Due to the ion−neurotransmitter−ion mechanism in IONTRONIC DEVICES chemical synapses, it was revealed that synaptic characteristics Toward simulating synaptic behaviors in neuronal networks could be regulated by the occurrence of synaptic events: the with synaptic iontronic devices for effective neuromorphic strength of synaptic junctions (i.e., synaptic weight), which is computing, understanding of the synaptic characteristics and related to the efficiency of information processing between how synaptic iontronic devices mimicked these characteristics neurons, changes with the occurrence of synaptic spikes; that is 39−41 should be taken into consideration at first. In this section, one synaptic plasticity. In biological synapses, synaptic of the most fundamental but important synaptic characteristics, plasticity is related to the cellular state of neurons, which is synaptic plasticity, which directly contributed to study and associated with the intracellular and extracellular environment, memory functions of the brain, was comprehensively reviewed such as the Ca2+-dependent nature of the neurotransmitter − to understand the role of ions in biological synapses and release process.42 45 This synaptic plasticity characteristic synaptic iontronic devices. And how to mimic synaptic contributed to the signal procession function of neurons by plasticity of different patterns with synaptic iontronic devices regulating the synapse weight between neurons and outputting 72 https://dx.doi.org/10.1021/acsabm.0c00806
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