Neurons in primary visual cortex have been characterized by their selectivity to orientation, spatiotemporal frequencies, and motion direction, among others all essential parameters to decompose complex image structure. However, their concerted functioning upon real-world visual dynamics remained unobserved since most studies tested these parameters in isolation rather than in rich mixture. We used voltage-sensitive dye imaging to characterize population responses to natural scene movies, and for comparison, to well-established moving gratings. For the latter, we confirm previous observations of a deceleration/acceleration notch. Upon stimulation with natural movies, however, a subsequent acceleration component was almost absent. Furthermore, we found that natural stimuli revealed sparsely distributed nonseparable space-time dynamics, continuously modulated by movie motion. Net excitation levels detected with gratings were reached only rarely with natural movies. Emphasizing this observation, across the entire time course, both average and peak amplitudes were lower than nonspecific, that is, minimum, activity obtained for gratings. We estimated a necessary increase of ∼30% of movie contrast to match high grating activity levels. Our results suggest that in contrast to gratings, processing of complex natural input is based on a balanced and stationary interplay between excitation and inhibition and point to the importance of suppressive mechanisms in shaping the operating regime of cortical dynamics.