Neuronal nonlinearity explains greater visual spatial resolution for darks than lights

Significance Light and dark stimuli are separately processed by ON and OFF channels in retina and thalamus. Although most textbooks assume that ON and OFF visual responses are relatively balanced throughout the visual system, recent studies have identified a pronounced overrepresentation of OFF responses in the cerebral cortex. This recent discovery resonates with Galileo and Helmholtz’s pioneering observations that visual spatial resolution is higher for darks than lights. In this paper, we demonstrate that these two seemingly separate findings are related and caused by a pronounced difference between ON and OFF luminance response functions, which most likely originates in photoreceptors. Therefore, asymmetric ON and OFF neural responses provide the neurophysiological explanation for an almost four-century-old puzzle dating back to Galileo. 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 ON-center 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.