Unstructured network topology begets order-based representation by privileged neurons

How spiking activity reverberates through neuronal networks, how evoked and spontaneous activity interacts and blends, 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 subpopulation of ‘pioneer neurons’ that, by their firing order, reliably encode previous external stimulation. We also confirm that pioneer neurons are ‘sensitive’ in that they are recruited by small fluctuations of population activity. We show that order-based representations rely on a ‘chain’ of pioneer neurons with different degrees of sensitivity and thus constitute an emergent property of collective dynamics. The forming of such representations is greatly favoured by a broadly heterogeneous connection topology—a broad ‘middle class’ in degree of connectedness. In conclusion, we offer a minimal model for the representational role of pioneer neurons, as observed experimentally in vitro. In addition, we show that broadly heterogeneous connectivity enhances the representational capacity of unstructured networks. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1007/s00422-020-00819-9) contains supplementary material, which is available to authorized users.