Heterogeneity of synaptic input connectivity regulates spike-based neuronal avalanches

Our mysterious brain is believed to operate near a non-equilibrium point and generate critical self-organized avalanches in neuronal activity. A central topic in neuroscience is to elucidate the underlying circuitry mechanisms of neuronal avalanches in the brain. Recent experimental evidence has revealed significant heterogeneity in both synaptic input and output connectivity, but whether the structural heterogeneity participates in the regulation of neuronal avalanches remains poorly understood. By computational modeling, we predict that different types of structural heterogeneity contribute distinct effects on avalanche neurodynamics. In particular, neuronal avalanches can be triggered at an intermediate level of input heterogeneity, but heterogeneous output connectivity cannot evoke avalanche dynamics. In the criticality region, the co-emergence of multi-scale cortical activities is observed, and both the avalanche dynamics and neuronal oscillations are modulated by the input heterogeneity. Remarkably, we show similar results can be reproduced in networks with various types of in- and out-degree distributions. Overall, these findings not only provide details on the underlying circuitry mechanisms of nonrandom synaptic connectivity in the regulation of neuronal avalanches, but also inspire testable hypotheses for future experimental studies.