Abstract
Brain-inspired computing hardware aims to emulate the structure and working principles of the brain and could be used to address current limitations in artificial intelligence technologies. However, brain-inspired silicon chips are still limited in their ability to fully mimic brain function as most examples are built on digital electronic principles. Here we report an artificial intelligence hardware approach that uses adaptive reservoir computation of biological neural networks in a brain organoid. In this approach—which is termed Brainoware—computation is performed by sending and receiving information from the brain organoid using a high-density multielectrode array. By applying spatiotemporal electrical stimulation, nonlinear dynamics and fading memory properties are achieved, as well as unsupervised learning from training data by reshaping the organoid functional connectivity. We illustrate the practical potential of this technique by using it for speech recognition and nonlinear equation prediction in a reservoir computing framework.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
Source data are provided with this paper. All other data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Tang, J. et al. Bridging biological and artificial neural networks with emerging neuromorphic devices: fundamentals, progress, and challenges. Adv. Mater. 31, e1902761 (2019).
Sejnowski, T. J. & Rosenberg, C. R. Parallel networks that learn to pronounce English text. Complex Syst. 1, 145–168 (1987).
Samarasinghe, S. Neural Networks for Applied Sciences and Engineering: From Fundamentals to Complex Pattern Recognition (Auerbach Publications, 2016).
Gokmen, T. & Vlasov, Y. Acceleration of deep neural network training with resistive cross-point devices: design considerations. Front. Neurosci. 10, 333 (2016).
Mehonic, A. & Kenyon, A. J. Brain-inspired computing needs a master plan. Nature 604, 255–260 (2022).
Xia, Q. & Yang, J. J. Memristive crossbar arrays for brain-inspired computing. Nat. Mater. 18, 309–323 (2019).
Wang, Z. R. et al. Resistive switching materials for information processing. Nat. Rev. Mater. 5, 173–195 (2020).
Tanaka, G. et al. Recent advances in physical reservoir computing: a review. Neural Netw. 115, 100–123 (2019).
Zidan, M. A., Strachan, J. P. & Lu, W. D. The future of electronics based on memristive systems. Nat. Electron. 1, 22–29 (2018).
Grollier, J. et al. Neuromorphic spintronics. Nat. Electron. 3, 360–370 (2020).
Marković, D., Mizrahi, A., Querlioz, D. & Grollier, J. Physics for neuromorphic computing. Nat. Rev. Phys. 2, 499–510 (2020).
Goswami, S. et al. Decision trees within a molecular memristor. Nature 597, 51–56 (2021).
Purves, D. et al. Neurosciences (De Boeck Supérieur, 2019).
Parisi, G. I., Kemker, R., Part, J. L., Kanan, C. & Wermter, S. Continual lifelong learning with neural networks: a review. Neural Netw. 113, 54–71 (2019).
Krogh, A. What are artificial neural networks? Nat. Biotechnol. 26, 195–197 (2008).
Schmidhuber, J. Deep learning in neural networks: an overview. Neural Netw. 61, 85–117 (2015).
Milano, G. et al. In materia reservoir computing with a fully memristive architecture based on self-organizing nanowire networks. Nat. Mater. 21, 195–202 (2022).
Sillin, H. O. et al. A theoretical and experimental study of neuromorphic atomic switch networks for reservoir computing. Nanotechnology 24, 384004 (2013).
Strukov, D. B., Snider, G. S., Stewart, D. R. & Williams, R. S. The missing memristor found. Nature 453, 80–83 (2008).
Torrejon, J. et al. Neuromorphic computing with nanoscale spintronic oscillators. Nature 547, 428–431 (2017).
Zhang, W. Q. et al. Neuro-inspired computing chips. Nat. Electron. 3, 371–382 (2020).
Wang, Z. et al. Memristors with diffusive dynamics as synaptic emulators for neuromorphic computing. Nat. Mater. 16, 101–108 (2017).
Yang, J. J., Strukov, D. B. & Stewart, D. R. Memristive devices for computing. Nat. Nanotechnol. 8, 13–24 (2013).
Yao, P. et al. Face classification using electronic synapses. Nat. Commun. 8, 15199 (2017).
Li, C. et al. Analogue signal and image processing with large memristor crossbars. Nat. Electron. 1, 52–59 (2018).
Moon, J. et al. Temporal data classification and forecasting using a memristor-based reservoir computing system. Nat. Electron. 2, 480–487 (2019).
Zhong, Y. et al. Dynamic memristor-based reservoir computing for high-efficiency temporal signal processing. Nat. Commun. 12, 408 (2021).
Trujillo, C. A. et al. Complex oscillatory waves emerging from cortical organoids model early human brain network development. Cell Stem Cell 25, 558–569 (2019).
Lancaster, M. A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373–379 (2013).
Chiaradia, I. & Lancaster, M. A. Brain organoids for the study of human neurobiology at the interface of in vitro and in vivo. Nat. Neurosci. 23, 1496–1508 (2020).
Qian, X. et al. Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165, 1238–1254 (2016).
Lukoševičius, M. & Jaeger, H. Reservoir computing approaches to recurrent neural network training. Comput. Sci. Rev. 3, 127–149 (2009).
Giandomenico, S. L. et al. Cerebral organoids at the air-liquid interface generate diverse nerve tracts with functional output. Nat. Neurosci. 22, 669–679 (2019).
Sharf, T. et al. Functional neuronal circuitry and oscillatory dynamics in human brain organoids. Nat. Commun. 13, 4403 (2022).
Canossa, M. et al. Neurotrophin release by neurotrophins: implications for activity-dependent neuronal plasticity. Proc. Natl Acad. Sci. USA 94, 13279–13286 (1997).
Smirnova, L. et al. Organoid intelligence (OI): the new frontier in biocomputing and intelligence-in-a-dish. Front. Sci. 1, 1017235 (2023).
Magliaro, C. & Ahluwalia, A. To brain or not to brain organoids. Front. Sci. 1, 1148873 (2023).
Hofer, M. & Lutolf, M. P. Engineering organoids. Nat. Rev. Mater. 6, 402–420 (2021).
Huang, Q. et al. Shell microelectrode arrays (MEAs) for brain organoids. Sci. Adv. 8, eabq5031 (2022).
Park, Y. et al. Three-dimensional, multifunctional neural interfaces for cortical spheroids and engineered assembloids. Sci. Adv. 7, eabf9153 (2021).
Li, T. L. et al. Stretchable mesh microelectronics for the biointegration and stimulation of human neural organoids. Biomaterials 290, 121825 (2022).
Weltman, A., Yoo, J. & Meng, E. Flexible, penetrating brain probes enabled by advances in polymer microfabrication. Micromachines 7, 180 (2016).
Lin, S. et al. A flexible, robust, and gel-free electroencephalogram electrode for noninvasive brain-computer interfaces. Nano Lett. 19, 6853–6861 (2019).
Kagan, B. J. et al. In vitro neurons learn and exhibit sentience when embodied in a simulated game-world. Neuron 110, 3952–3969.e3958 (2022).
Bakkum, D. J., Chao, Z. C. & Potter, S. M. Spatio-temporal electrical stimuli shape behavior of an embodied cortical network in a goal-directed learning task. J. Neural Eng. 5, 310 (2008).
Chao, Z. C., Bakkum, D. J. & Potter, S. M. Shaping embodied neural networks for adaptive goal-directed behavior. PLoS Comput. Biol. 4, e1000042 (2008).
Ao, Z. et al. Understanding immune-driven brain aging by human brain organoid microphysiological analysis platform. Adv. Sci. 9, e2200475 (2022).
Acknowledgements
F.G. wants to acknowledge support from the National Institute of Health Awards (DP2AI160242, R01DK133864 and U01DA056242). We also acknowledge Indiana University Imaging Center (NIH1S10OD024988-01).
Author information
Authors and Affiliations
Contributions
F.G. and H.C. conceived the study and designed the experiments. H.C., Z.A., C.T. and Z.W. performed the experiment. H.C., H.L., J.T., M.G. and K.M. analysed the data. F.G. and H.C. wrote the paper. All authors read and provided feedback on the paper.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Nature Electronics thanks Arti Ahluwalia and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Figs. 1–11, Tables 1–3, Discussion and References.
Supplementary Video 1
Electrical activity of an organoid. Spike-activity heat map of cortical organoid electrical activity (day 60, culture in an high-density MEA chip). The video is in ×4. Scale bar, 100 μm.
Supplementary Video 2
Calcium activity of an organoid. Confocal calcium imaging of organoid neural activity (day 60, transfer to a glass-bottom six-well plate). The video is in ×10. Scale bar, 100 μm.
Source data
Source Data Fig. 2
Statistical source data.
Source Data Fig. 3
Statistical source data.
Source Data Fig. 4
Statistical source data.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Cai, H., Ao, Z., Tian, C. et al. Brain organoid reservoir computing for artificial intelligence. Nat Electron 6, 1032–1039 (2023). https://doi.org/10.1038/s41928-023-01069-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41928-023-01069-w
This article is cited by
-
Neuroethics and AI ethics: a proposal for collaboration
BMC Neuroscience (2024)
-
Connectome-based reservoir computing with the conn2res toolbox
Nature Communications (2024)
-
Induced pluripotent stem cells (iPSCs): molecular mechanisms of induction and applications
Signal Transduction and Targeted Therapy (2024)
-
Biocomputing with organoid intelligence
Nature Reviews Bioengineering (2024)
-
BiœmuS: A new tool for neurological disorders studies through real-time emulation and hybridization using biomimetic Spiking Neural Network
Nature Communications (2024)