CRITICAL NEURONAL AVALANCHES ARISE 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 spontaneous neuronal avalanches exhibited critical-like dynamics at balanced E-I ratios but became smaller and shorter when the ratios were imbalanced, reflecting more ordered dynamics. 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. Together, these results demonstrate that excitatory–inhibitory balance shapes spontaneous neuronal avalanches in the zebrafish optic tectum in vivo, and support a mechanism in which critical neuronal avalanches emerge from balanced amplification in networks poised near criticality.