Broadly heterogeneous network topology begets order-based representation by privileged neurons

Abstract: How spiking activity reverberates through neuronal networks, how evoked and spontaneous activity interact and blend, and how the combined activities represent external stimulation are pivotal questions in neuroscience. We simulated minimal models of unstructured spiking networks in silico, asking whether and how gentle external stimulation might be subsequently reflected in spontaneous activity fluctuations. Consistent with earlier findings in silico and in vitro, we observe a privileged sub-population of 'pioneer neurons' that, by their firing order, reliably encode previous external stimulation. We show that the distinctive role of pioneer neurons is owed to a combination of exceptional sensitivity to, and pronounced influence on, network activity. We further show that broadly heterogeneous connection topology - a broad "middle class" in degree of connectedness - not only increases the number of 'pioneer neurons' in unstructured networks, but also renders the emergence of 'pioneer neurons' more robust to changes in the excitatory-inhibitory balance. In conclusion, we offer a minimal model for the emergence and representational role of 'pioneer neurons', as observed experimentally in vitro. In addition, we show how broadly heterogeneous connectivity can enhance the representational capacity of unstructured networks.