Dynamics and critical behaviour of neuronal cultures grown on topographical patterns with fractal structure

Abstract

Neuronal cultures are an excellent experimental tool to study the collective behaviour of neuronal ensembles, providing information on the principles of synaptic functioning and propagation. However, neurons cultured on flat surfaces present limitations in terms of their functionality, as they exhibit a synchronous dynamic behaviour that differs from the much richer repertoire of activity of the brain. In order to address this limitation and help developing better in vitro tools to model the brain, here we studied the capacity to break off synchrony by modulating the spatial arrangement of neurons in the substrate they grow. For that, we designed polydimethylsiloxane (PDMS) topographical patterns with fractal geometry and used them as the substrate to grow neurons, with the goal to break the isotropy in connectivity and enrich dynamics. Neuronal activity was recorded with calcium fluorescence imaging and data analysed in the context of criticality, which was inspired by recent findings suggesting that a rich structural connectivity in the brain is behind its functioning at the edge of criticality. We observed that, first, neurons cultured on fractal patterns exhibited richer and more complex dynamics as compared to standard cultures; and, second, that an analysis of the data using the renormalisation group approach, revealed the presence of scale invariance and typical features of systems poised at criticality. Our study is a multidisciplinary endeavour that combined experimental, theoretical and data analysis aspects to validate the hypothesis of the existence of a self-organised criticality in living neuronal networks, from cultures up to the brain.