Distributed network interactions and their emergence in developing neocortex

The principles governing the functional organization and development of long-range network interactions in the neocortex remain poorly understood. Using in vivo wide-field and 2-photon calcium imaging of spontaneous activity patterns in mature ferret visual cortex, we find widespread modular correlation patterns that accurately predict the local structure of visually-evoked orientation columns several millimeters away. Longitudinal imaging demonstrates that long-range spontaneous correlations are present early in cortical development prior to the elaboration of horizontal connections, and predict mature network structure. Silencing feed-forward drive through retinal or thalamic blockade does not eliminate early long-range correlated activity, suggesting a cortical origin. Circuit models containing only local, but heterogeneous, connections are sufficient to generate long-range correlated activity by confining activity patterns to a low-dimensional subspace via multi-synaptic short-range interactions. These results suggest that local connections in early cortical circuits can generate structured long-range network correlations that guide the formation of visually-evoked distributed functional networks.