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Critical dynamics arise during structured information presentation within embodied in vitro neuronal networks

Author

Listed:
  • Forough Habibollahi

    (Cortical Labs Pty Ltd
    University of Melbourne
    University of Melbourne)

  • Brett J. Kagan

    (Cortical Labs Pty Ltd)

  • Anthony N. Burkitt

    (University of Melbourne)

  • Chris French

    (University of Melbourne
    Royal Melbourne Hospital)

Abstract

Understanding how brains process information is an incredibly difficult task. Amongst the metrics characterising information processing in the brain, observations of dynamic near-critical states have generated significant interest. However, theoretical and experimental limitations associated with human and animal models have precluded a definite answer about when and why neural criticality arises with links from attention, to cognition, and even to consciousness. To explore this topic, we used an in vitro neural network of cortical neurons that was trained to play a simplified game of ‘Pong’ to demonstrate Synthetic Biological Intelligence (SBI). We demonstrate that critical dynamics emerge when neural networks receive task-related structured sensory input, reorganizing the system to a near-critical state. Additionally, better task performance correlated with proximity to critical dynamics. However, criticality alone is insufficient for a neuronal network to demonstrate learning in the absence of additional information regarding the consequences of previous actions. These findings offer compelling support that neural criticality arises as a base feature of incoming structured information processing without the need for higher order cognition.

Suggested Citation

  • Forough Habibollahi & Brett J. Kagan & Anthony N. Burkitt & Chris French, 2023. "Critical dynamics arise during structured information presentation within embodied in vitro neuronal networks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41020-3
    DOI: 10.1038/s41467-023-41020-3
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    References listed on IDEAS

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    1. Shree Hari Gautam & Thanh T Hoang & Kylie McClanahan & Stephen K Grady & Woodrow L Shew, 2015. "Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-15, December.
    2. Christian Meisel & Alexander Storch & Susanne Hallmeyer-Elgner & Ed Bullmore & Thilo Gross, 2012. "Failure of Adaptive Self-Organized Criticality during Epileptic Seizure Attacks," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-8, January.
    3. Jens Wilting & Viola Priesemann, 2018. "Inferring collective dynamical states from widely unobserved systems," Nature Communications, Nature, vol. 9(1), pages 1-7, December.
    4. Andreas Klaus & Shan Yu & Dietmar Plenz, 2011. "Statistical Analyses Support Power Law Distributions Found in Neuronal Avalanches," PLOS ONE, Public Library of Science, vol. 6(5), pages 1-12, May.
    5. Benjamin Cramer & David Stöckel & Markus Kreft & Michael Wibral & Johannes Schemmel & Karlheinz Meier & Viola Priesemann, 2020. "Control of criticality and computation in spiking neuromorphic networks with plasticity," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    6. Paolo Moretti & Miguel A. Muñoz, 2013. "Griffiths phases and the stretching of criticality in brain networks," Nature Communications, Nature, vol. 4(1), pages 1-10, December.
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