Critical neuronal avalanches emerge from excitation-inhibition balanced spontaneous activity

Neuronal avalanches are sequences of neural activations that exhibit scale-invariant statistics, suggesting neural activity operates near a critical point. Theoretical studies proposed that the balance between excitation (E) and inhibition (I), along with neuromodulation, are key factors influencing this critical behavior. Here, we performed in-vivo studies to investigate the role of E and I neurons in generating neuronal avalanches in the optic tectum of zebrafish larvae. For this, we used double-transgenic zebrafish larvae expressing cell-type-specific fluorescent proteins and GCaMP6f, combined with immunostaining and selective-plane illumination microscopy to monitor spontaneous neuronal activity and neurotransmitter identity. We found that neural activity approached criticality at balanced E-I ratios but became disordered when E-I ratios were imbalanced. A stochastic network model operating at a critical point, where excitation and inhibition couplings are balanced and balanced amplification drives network avalanches, successfully reproduced the observed statistics of neuronal avalanches and their dependence on E-I ratio fluctuations.