Local field potentials and the underlying endogenous electric fields (EFs) are traditionally considered to be epiphenomena of structured neuronal network activity. Recently, however, externally applied EFs have been shown to modulate pharmacologically evoked network activity in rodent hippocampus. In contrast, very little is known about the role of endogenous EFs during physiological activity states in neocortex. Here, we used the neocortical slow oscillation in vitro as a model system to show that weak sinusoidal and naturalistic EFs enhance and entrain physiological neocortical network activity with an amplitude threshold within the range of in vivo endogenous field strengths. Modulation of network activity by positive and negative feedback fields based on the network activity in real-time provide direct evidence for a feedback loop between neuronal activity and endogenous EF. This significant susceptibility of active networks to EFs that only cause small changes in membrane potential in individual neurons suggests that endogenous EFs could guide neocortical network activity.