The temporal frequency of synaptic activation is a decisive factor in the regulation of perceptual detection thresholds following high or low frequency sensory stimulation. However, surprisingly little is known about the neuronal and circuit level responses to distinct temporal parameters of sensory input. Here we demonstrate that the temporal frequency of a visual stimulus determines the locus of expression and specificity of visual response potentiation. Repetitive high frequency stimulation (HFS, 20 Hz), but not low frequency stimulation (LFS, 2 Hz), suppresses the activity of fast-spiking interneurons, and primes ongoing gamma oscillatory rhythms for visually-evoked phase reset. Accordingly, visual stimulation subsequent to HFS induces a non-stimulus specific response potentiation that is expressed in all cortical layers. In contrast, LFS induces a stimulus specific response potentiation that is specifically expressed in layer 4. This generalized response potentiation induced by HFS is coincident with an improved performance in a visual detection task that generalizes to novel visual stimuli.