Development of neural population activity toward self-organized criticality

Self-organized criticality (SoC), a spontaneous dynamic state established and maintained in networks of moderate complexity, is a universal characteristic of neural systems. Such systems produce cascades of spontaneous activity that are typically characterized by power-law distributions and rich, stable spatiotemporal patterns (i.e., neuronal avalanches). Since the dynamics of the critical state confer advantages in information processing within neuronal networks, it is of great interest to determine how criticality emerges during development. One possible mechanism is developmental, and includes axonal elongation during synaptogenesis and subsequent synaptic pruning in combination with the maturation of GABAergic inhibition (i.e., the integration then fragmentation process). Because experimental evidence for this mechanism remains inconclusive, we studied the developmental variation of neuronal avalanches in dissociated cortical neurons using high-density complementary metal-oxide semiconductor (CMOS) microelectrode arrays (MEAs). The spontaneous activities of nine cultures were monitored using CMOS MEAs from 4 to 30days in vitro (DIV) at single-cell spatial resolution. While cells were immature, cultures demonstrated random-like patterns of activity and an exponential avalanche size distribution; this distribution was followed by a bimodal distribution, and finally a power-law-like distribution. The bimodal distribution was associated with a large-scale avalanche with a homogeneous spatiotemporal pattern, while the subsequent power-law distribution was associated with diverse patterns. These results suggest that the SoC emerges through a two-step process: the integration process accompanying the characteristic large-scale avalanche and the fragmentation process associated with diverse middle-size avalanches.