Critical neuronal avalanches arise from excitation-inhibition balanced spontaneous activity

Neuronal avalanches are sequences of neural activations exhibiting scale-invariant statistics, indicative of critical dynamics. 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 exhibited avalanches with critical exponents at balanced and slightly excitation-dominated E-I ratios, whereas imbalanced ratios led to faster-decaying avalanches. A stochastic network model operating at a critical point, where excitation and inhibition couplings are balanced and balanced amplification drives network avalanches, reproduced the observed statistics of neuronal avalanches and their dependence on E-I ratio fluctuations.