Distributed network interactions and their emergence in developing neocortex

The cortical networks that underlie behavior exhibit an orderly functional organization at local and global scales, which is readily evident in the visual cortex of carnivores and primates. Here, neighboring columns of neurons represent the full range of stimulus orientations and contribute to distributed networks spanning several millimeters. However, the principles governing functional interactions that bridge this fine-scale functional architecture and distant network elements are unclear, and the emergence of these network interactions during development remains unexplored.

Here, by imaging spontaneous activity patterns in mature ferret visual cortex, we find widespread and specific modular correlation patterns that accurately predict the local structure of visually-evoked orientation columns from the spontaneous activity of neurons that lie several millimeters away. The large-scale networks revealed by correlated spontaneous activity show abrupt ‘fractures’ in continuity that are in tight register with evoked orientation pinwheels. Chronic in vivo imaging demonstrates that these large-scale modular correlation patterns and fractures are already present at early stages of cortical development and predictive of the mature network structure. Silencing feed-forward drive through either retinal or thalamic blockade does not affect network structure suggesting a cortical origin for this large-scale correlated activity, despite the immaturity of long-range horizontal network connections in the early cortex. Using a circuit model containing only local connections, we demonstrate that such a circuit is sufficient to generate large-scale correlated activity, while also producing other key features of spontaneous activity, all in close agreement with our empirical data. These results demonstrate the precise local and global organization of cortical networks revealed through correlated spontaneous activity and suggest that local connections in early cortical circuits generate structured long-range network correlations that underlie the subsequent formation of visually-evoked distributed functional networks.