AbstractThe interactions between areas of the neocortex are fluid and state-dependent, but how individual neurons couple to cortex-wide network dynamics remains poorly understood. We correlated the spiking of individual neurons in primary visual (V1) and retrosplenial (RSP) cortex to activity across dorsal cortex, recorded simultaneously by calcium imaging. Individual neurons were correlated with distinct and reproducible patterns of activity across the cortical surface; while some fired predominantly with their local area, others coupled to activity in subsets of distal areas. The extent of distal coupling was predicted by how strongly neurons correlated with the local network. Changes in brain state triggered by locomotion re-structured how neurons couple to cortical activity patterns: running strengthened affiliations of V1 neurons with visual areas, while strengthening distal affiliations of RSP neurons with sensory cortices. Thus, individual neurons within a cortical area can independently engage in different cortical networks depending on the animal's behavioral state.