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Cortical neurons are characterized by their variable spiking patterns. Here, we examine the specific hypothesis that cortical synchrony drives spiking variability in vivo. Using dynamic clamps, we demonstrate that intrinsic neuronal properties do not contribute substantially to spiking variability, but rather spiking variability emerges from weakly synchronous network drive. With large-scale electrophysiology, we quantify the degree of synchrony and its timescale in cortical networks in vivo. The timescale of synchrony shifts in a range from 25 to 200 ms, depending on the presence of external sensory input. In particular, when the network moves from spontaneous to driven modes, the synchrony timescales shift from slow to fast, leading to a natural reduction in response variability across cortical areas. Finally, while an individual neuron exhibits reliable responses to physiological drive, different neurons respond in a distinct fashion according to their intrinsic properties, contributing to stable synchrony across the neural network.