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ORIGINAL RESEARCH article
Front. Neural Circuits
Volume 18 - 2024 |
doi: 10.3389/fncir.2024.1456558
This article is part of the Research Topic Bridging Computation, Biophysics, Medicine, and Engineering in Neural Circuits View all 4 articles
Criticality and universality in neuronal cultures during 'up' and 'down' states
Provisionally accepted- 1 University of Calgary, Calgary, Canada
- 2 McGill University, Montreal, Quebec, Canada
The brain can be seen as a self-organized dynamical system that optimizes information processing and storage capabilities. This is supported by studies across scales, from small neuronal assemblies to the whole brain, where neuronal activity exhibits features typically associated with phase transitions in statistical physics. Such a critical state is characterized by the emergence of scale-free statistics as captured, for example, by the sizes and durations of activity avalanches corresponding to a cascading process of information flow. Another phenomenon observed during sleep, under anesthesia, and in in vitro cultures, is that cortical and hippocampal neuronal networks alternate between "up" and "down" states characterized by very distinct firing rates. Previous theoretical work has been able to relate these two concepts and proposed that only up states are critical whereas down states are subcritical, also indicating that the brain spontaneously transitions between the two. Using high-speed high-resolution calcium imaging recordings of neuronal cultures, we test this hypothesis here by analyzing the neuronal avalanche statistics in populations of thousands of neurons during "up" and "down" states separately. We find that both "up" and "down" states can exhibit scale-free behavior when taking into account their intrinsic time scales. In particular, the statistical signature of "down" states is indistinguishable from those observed previously in cultures without "up" states. We show that such behavior can not be explained by network models of non-conservative leaky integrate-andfire neurons with short-term synaptic depression, even when realistic noise levels, spatial network embeddings, and heterogeneous populations are taken into account, which instead exhibits behavior consistent with previous theoretical models. Similar differences were also observed when taking into consideration finite-size scaling effects, suggesting that the intrinsic dynamics and self-organization mechanisms of these cultures might be more complex than previously thought. In particular, our findings point to the existence of different mechanisms of neuronal communication, with different time scales, acting during either high-activity or low-activity states, potentially requiring different plasticity mechanisms.
Keywords: up and down states, critical brain dynamics, neuronal avalanches, Dissociated cultures, self-organization mechanisms in neuronal systems
Received: 28 Jun 2024; Accepted: 19 Aug 2024.
Copyright: © 2024 Yaghoubi, Orlandi, Colicos and Davidsen. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
* Correspondence:
Joern Davidsen, University of Calgary, Calgary, Canada
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