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How spiking activity reverberates through neuronal networks, how evoked andspontaneous activity interact and blend, and how the combined activitiesrepresent external stimulation are pivotal questions in neuroscience. Wesimulated minimal models of unstructured spiking networks in silico, askingwhether and how gentle external stimulation might be subsequently reflected inspontaneous activity fluctuations. Consistent with earlier findings in silicoand in vitro, we observe a privileged sub-population of 'pioneer neurons' that,by their firing order, reliably encode previous external stimulation. We showthat the distinctive role of pioneer neurons is owed to a combination ofexceptional sensitivity to, and pronounced influence on, network activity. Wefurther show that broadly heterogeneous connection topology - a broad "middleclass" in degree of connectedness - not only increases the number of 'pioneerneurons' in unstructured networks, but also renders the emergence of 'pioneerneurons' more robust to changes in the excitatory-inhibitory balance. Inconclusion, we offer a minimal model for the emergence and representationalrole of 'pioneer neurons', as observed experimentally in vitro. In addition, weshow how broadly heterogeneous connectivity can enhance the representationalcapacity of unstructured networks.

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