Identification of brain-like functional information architectures in embryonic tissue of Xenopus laevis.
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Understanding how populations of cells collectively coordinate activity to produce the complex structures and behaviors that characterize multicellular organisms is a fundamental issue in modern biology. Here we show how mathematical techniques from complex systems science and multivariate information theory can provide a rigorous framework for inferring the structure of collective organization in non-neural tissue. Many of these techniques were developed and refined in the context of theoretical neuroscience, a field well-used to the problem of inferring coordinated activity in high-dimensional data. In neuroscience, these statistics (functional connectivity network structure, modularity, higher-order information, etc) have been found to be altered during different cognitive, clinical, or behavioral states and are generally thought to be informative about the underlying dynamics linking biology to cognition. Here we show that these same patterns of coordinated activity are also present in the aneural tissues of evolutionarily distant biological systems: preparations of self-motile embryonic Xenopus tissue (colloquially known as "basal Xenobots". When analyzing calcium recordings from basal Xenobots and comparing them to fMRI recordings from a sample of adult human brains, we find that the bots have a "brain-like functional information architecture, complete with positive and negative functional connections, meso-scale communities, higher-order redundant and synergistic interactions, and integrated information that is "greater than the sum of its parts". By comparing each recording (brain and bot) to a personalized null model that preserves all first-order statistical structures (autocorrelation, frequency spectrum, etc. ) while disrupting all higher-order interactions, we show that these are genuine higher order interactions and not trivially reducible to lower-order features of the data. These similarities suggest that such patterns of activity and information structures either: arose independently in these two systems epithelial constructs and brains, are epiphenomenological byproducts of other dynamics conserved across vastly different configurations of life; or somehow directly support adaptive behavior across diverse living systems.