IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-49668-1.html
   My bibliography  Save this article

Unravelling the operation of organic artificial neurons for neuromorphic bioelectronics

Author

Listed:
  • Pietro Belleri

    (University of Brescia)

  • Judith Pons i Tarrés

    (Max Planck Institute for Polymer Research)

  • Iain McCulloch

    (University of Oxford)

  • Paul W. M. Blom

    (Max Planck Institute for Polymer Research)

  • Zsolt M. Kovács-Vajna

    (University of Brescia)

  • Paschalis Gkoupidenis

    (Max Planck Institute for Polymer Research
    North Carolina State University
    North Carolina State University)

  • Fabrizio Torricelli

    (University of Brescia)

Abstract

Organic artificial neurons operating in liquid environments are crucial components in neuromorphic bioelectronics. However, the current understanding of these neurons is limited, hindering their rational design and development for realistic neuronal emulation in biological settings. Here we combine experiments, numerical non-linear simulations, and analytical tools to unravel the operation of organic artificial neurons. This comprehensive approach elucidates a broad spectrum of biorealistic behaviors, including firing properties, excitability, wetware operation, and biohybrid integration. The non-linear simulations are grounded in a physics-based framework, accounting for ion type and ion concentration in the electrolytic medium, organic mixed ionic-electronic parameters, and biomembrane features. The derived analytical expressions link the neurons spiking features with material and physical parameters, bridging closer the domains of artificial neurons and neuroscience. This work provides streamlined and transferable guidelines for the design, development, engineering, and optimization of organic artificial neurons, advancing next generation neuronal networks, neuromorphic electronics, and bioelectronics.

Suggested Citation

  • Pietro Belleri & Judith Pons i Tarrés & Iain McCulloch & Paul W. M. Blom & Zsolt M. Kovács-Vajna & Paschalis Gkoupidenis & Fabrizio Torricelli, 2024. "Unravelling the operation of organic artificial neurons for neuromorphic bioelectronics," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49668-1
    DOI: 10.1038/s41467-024-49668-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-49668-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-49668-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Thomas F. Schranghamer & Aaryan Oberoi & Saptarshi Das, 2020. "Graphene memristive synapses for high precision neuromorphic computing," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    2. Suhas Kumar & R. Stanley Williams & Ziwen Wang, 2020. "Third-order nanocircuit elements for neuromorphic engineering," Nature, Nature, vol. 585(7826), pages 518-523, September.
    3. Paolo Romele & Matteo Ghittorelli & Zsolt Miklós Kovács-Vajna & Fabrizio Torricelli, 2019. "Ion buffering and interface charge enable high performance electronics with organic electrochemical transistors," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    4. M. Prezioso & F. Merrikh-Bayat & B. D. Hoskins & G. C. Adam & K. K. Likharev & D. B. Strukov, 2015. "Training and operation of an integrated neuromorphic network based on metal-oxide memristors," Nature, Nature, vol. 521(7550), pages 61-64, May.
    5. Matteo Ghittorelli & Leona Lingstedt & Paolo Romele & N. Irina Crăciun & Zsolt Miklós Kovács-Vajna & Paul W. M. Blom & Fabrizio Torricelli, 2018. "High-sensitivity ion detection at low voltages with current-driven organic electrochemical transistors," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    6. Ibrahim Fakih & Oliver Durnan & Farzaneh Mahvash & Ilargi Napal & Alba Centeno & Amaia Zurutuza & Viviane Yargeau & Thomas Szkopek, 2020. "Selective ion sensing with high resolution large area graphene field effect transistor arrays," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    7. Kamal Abu-Hassan & Joseph D. Taylor & Paul G. Morris & Elisa Donati & Zuner A. Bortolotto & Giacomo Indiveri & Julian F. R. Paton & Alain Nogaret, 2019. "Optimal solid state neurons," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    8. Mingyi Rao & Hao Tang & Jiangbin Wu & Wenhao Song & Max Zhang & Wenbo Yin & Ye Zhuo & Fatemeh Kiani & Benjamin Chen & Xiangqi Jiang & Hefei Liu & Hung-Yu Chen & Rivu Midya & Fan Ye & Hao Jiang & Zhong, 2023. "Thousands of conductance levels in memristors integrated on CMOS," Nature, Nature, vol. 615(7954), pages 823-829, March.
    9. Jacob Torrejon & Mathieu Riou & Flavio Abreu Araujo & Sumito Tsunegi & Guru Khalsa & Damien Querlioz & Paolo Bortolotti & Vincent Cros & Kay Yakushiji & Akio Fukushima & Hitoshi Kubota & Shinji Yuasa , 2017. "Neuromorphic computing with nanoscale spintronic oscillators," Nature, Nature, vol. 547(7664), pages 428-431, July.
    10. Alexander Serb & Johannes Bill & Ali Khiat & Radu Berdan & Robert Legenstein & Themis Prodromakis, 2016. "Unsupervised learning in probabilistic neural networks with multi-state metal-oxide memristive synapses," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    11. Padinhare Cholakkal Harikesh & Chi-Yuan Yang & Deyu Tu & Jennifer Y. Gerasimov & Abdul Manan Dar & Adam Armada-Moreira & Matteo Massetti & Renee Kroon & David Bliman & Roger Olsson & Eleni Stavrinidou, 2022. "Organic electrochemical neurons and synapses with ion mediated spiking," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    12. Suhas Kumar & John Paul Strachan & R. Stanley Williams, 2017. "Chaotic dynamics in nanoscale NbO2 Mott memristors for analogue computing," Nature, Nature, vol. 548(7667), pages 318-321, August.
    13. Wei Yi & Kenneth K. Tsang & Stephen K. Lam & Xiwei Bai & Jack A. Crowell & Elias A. Flores, 2018. "Biological plausibility and stochasticity in scalable VO2 active memristor neurons," Nature Communications, Nature, vol. 9(1), pages 1-10, December.
    14. Paolo Romele & Paschalis Gkoupidenis & Dimitrios A. Koutsouras & Katharina Lieberth & Zsolt M. Kovács-Vajna & Paul W. M. Blom & Fabrizio Torricelli, 2020. "Multiscale real time and high sensitivity ion detection with complementary organic electrochemical transistors amplifier," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    15. Dmitri B. Strukov & Gregory S. Snider & Duncan R. Stewart & R. Stanley Williams, 2008. "The missing memristor found," Nature, Nature, vol. 453(7191), pages 80-83, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ushakov, Yury & Akther, Amir & Borisov, Pavel & Pattnaik, Debi & Savel’ev, Sergey & Balanov, Alexander G., 2021. "Deterministic mechanisms of spiking in diffusive memristors," Chaos, Solitons & Fractals, Elsevier, vol. 149(C).
    2. Ke Yang & Yanghao Wang & Pek Jun Tiw & Chaoming Wang & Xiaolong Zou & Rui Yuan & Chang Liu & Ge Li & Chen Ge & Si Wu & Teng Zhang & Ru Huang & Yuchao Yang, 2024. "High-order sensory processing nanocircuit based on coupled VO2 oscillators," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Dong, Yujiao & Yang, Shuting & Liang, Yan & Wang, Guangyi, 2022. "Neuromorphic dynamics near the edge of chaos in memristive neurons," Chaos, Solitons & Fractals, Elsevier, vol. 160(C).
    4. Sang Hyun Sung & Tae Jin Kim & Hyera Shin & Tae Hong Im & Keon Jae Lee, 2022. "Simultaneous emulation of synaptic and intrinsic plasticity using a memristive synapse," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Ushakov, Yury & Balanov, Alexander & Savel’ev, Sergey, 2021. "Role of noise in spiking dynamics of diffusive memristor driven by heating-cooling cycles," Chaos, Solitons & Fractals, Elsevier, vol. 145(C).
    6. Zhou, Wei & Jin, Peipei & Dong, Yujiao & Liang, Yan & Wang, Guangyi, 2023. "Memristor neurons and their coupling networks based on Edge of Chaos Kernel," Chaos, Solitons & Fractals, Elsevier, vol. 177(C).
    7. Xu, Quan & Wang, Yiteng & Wu, Huagan & Chen, Mo & Chen, Bei, 2024. "Periodic and chaotic spiking behaviors in a simplified memristive Hodgkin-Huxley circuit," Chaos, Solitons & Fractals, Elsevier, vol. 179(C).
    8. Ying, Jiajie & Min, Fuhong & Wang, Guangyi, 2023. "Neuromorphic behaviors of VO2 memristor-based neurons," Chaos, Solitons & Fractals, Elsevier, vol. 175(P2).
    9. Mingrui Jiang & Keyi Shan & Chengping He & Can Li, 2023. "Efficient combinatorial optimization by quantum-inspired parallel annealing in analogue memristor crossbar," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. Rui Wang & Tuo Shi & Xumeng Zhang & Jinsong Wei & Jian Lu & Jiaxue Zhu & Zuheng Wu & Qi Liu & Ming Liu, 2022. "Implementing in-situ self-organizing maps with memristor crossbar arrays for data mining and optimization," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    11. Ui Yeon Won & Quoc An Vu & Sung Bum Park & Mi Hyang Park & Van Dam Do & Hyun Jun Park & Heejun Yang & Young Hee Lee & Woo Jong Yu, 2023. "Multi-neuron connection using multi-terminal floating–gate memristor for unsupervised learning," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Fanfan Li & Dingwei Li & Chuanqing Wang & Guolei Liu & Rui Wang & Huihui Ren & Yingjie Tang & Yan Wang & Yitong Chen & Kun Liang & Qi Huang & Mohamad Sawan & Min Qiu & Hong Wang & Bowen Zhu, 2024. "An artificial visual neuron with multiplexed rate and time-to-first-spike coding," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    13. Padinhare Cholakkal Harikesh & Chi-Yuan Yang & Deyu Tu & Jennifer Y. Gerasimov & Abdul Manan Dar & Adam Armada-Moreira & Matteo Massetti & Renee Kroon & David Bliman & Roger Olsson & Eleni Stavrinidou, 2022. "Organic electrochemical neurons and synapses with ion mediated spiking," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    14. Ren, Lujie & Mou, Jun & Banerjee, Santo & Zhang, Yushu, 2023. "A hyperchaotic map with a new discrete memristor model: Design, dynamical analysis, implementation and application," Chaos, Solitons & Fractals, Elsevier, vol. 167(C).
    15. Kafraj, Mohadeseh Shafiei & Parastesh, Fatemeh & Jafari, Sajad, 2020. "Firing patterns of an improved Izhikevich neuron model under the effect of electromagnetic induction and noise," Chaos, Solitons & Fractals, Elsevier, vol. 137(C).
    16. Hakseung Rhee & Gwangmin Kim & Hanchan Song & Woojoon Park & Do Hoon Kim & Jae Hyun In & Younghyun Lee & Kyung Min Kim, 2023. "Probabilistic computing with NbOx metal-insulator transition-based self-oscillatory pbit," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    17. Tianyu Wang & Jialin Meng & Xufeng Zhou & Yue Liu & Zhenyu He & Qi Han & Qingxuan Li & Jiajie Yu & Zhenhai Li & Yongkai Liu & Hao Zhu & Qingqing Sun & David Wei Zhang & Peining Chen & Huisheng Peng & , 2022. "Reconfigurable neuromorphic memristor network for ultralow-power smart textile electronics," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    18. Yijun Li & Jianshi Tang & Bin Gao & Jian Yao & Anjunyi Fan & Bonan Yan & Yuchao Yang & Yue Xi & Yuankun Li & Jiaming Li & Wen Sun & Yiwei Du & Zhengwu Liu & Qingtian Zhang & Song Qiu & Qingwen Li & He, 2023. "Monolithic three-dimensional integration of RRAM-based hybrid memory architecture for one-shot learning," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    19. Panin, Gennady N., 2021. "Optoelectronic dynamic memristor systems based on two-dimensional crystals," Chaos, Solitons & Fractals, Elsevier, vol. 142(C).
    20. Peng Chen & Fenghao Liu & Peng Lin & Peihong Li & Yu Xiao & Bihua Zhang & Gang Pan, 2023. "Open-loop analog programmable electrochemical memory array," Nature Communications, Nature, vol. 14(1), pages 1-9, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49668-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.