Astronomers and physicists noticed centuries ago that visual spatial resolution is higher for dark than light stimuli, but the neuronal mechanisms for this perceptual asymmetry remain unknown. Here we demonstrate that the asymmetry is caused by a neuronal nonlinearity in the early visual pathway. We show that neurons driven by darks (OFF neurons) increase their responses roughly linearly with luminance decrements, independent of the background luminance. However, neurons driven by lights (ON neurons) saturate their responses with small increases in luminance and need bright backgrounds to approach the linearity of OFF neurons. We show that, as a consequence of this difference in linearity, receptive fields are larger in ON than OFF thalamic neurons, and cortical neurons are more strongly driven by darks than lights at low spatial frequencies. This ON/OFF asymmetry in linearity could be demonstrated in the visual cortex of cats, monkeys, and humans and in the cat visual thalamus. Furthermore, in the cat visual thalamus, we show that the neuronal nonlinearity is present at the ON receptive field center of ONcenter neurons and ON receptive field surround of OFF-center neurons, suggesting an origin at the level of the photoreceptor. These results demonstrate a fundamental difference in visual processing between ON and OFF channels and reveal a competitive advantage for OFF neurons over ON neurons at low spatial frequencies, which could be important during cortical development when retinal images are blurred by immature optics in infant eyes.neuronal coding | lateral geniculate nucleus | area V1 | irradiation illusion | LFP L ight and dark stimuli are separately processed by ON and OFF channels in the retina and visual thalamus. Surprisingly, although most textbooks assume that ON and OFF visual responses are balanced throughout the visual system, recent studies have identified a pronounced overrepresentation of the OFF visual responses in primary visual cortex (area V1) (1-3). This recent discovery resonates with pioneering studies by Galilei (4) and von Helmholtz (5) who noticed that visual spatial resolution was higher for dark than light stimuli. Galilei (4) related the difference in resolution to the observation that a light patch on a dark background appears larger than the same sized dark patch on a light background, an illusion that von Helmholtz (5) named the "irradiation illusion." Although this illusion has been studied in the past (6, 7), its underlying neuronal mechanisms remain unknown. It has been suggested that the perceived size differences could be caused by the light scatter in the optics of the eye followed by a neuronal nonlinearity (6, 7), but there are no neuronal measurements of a nonlinearity that fits the explanation. Previous studies revealed differences in response linearity between ON and OFF retinal ganglion cells (8, 9) and horizontal cells (10). However, a main conclusion from these studies was that ON retinal ganglion cells were roughly linear and less rectified than OFF retinal gangl...