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...

SUMMARY Visual information is mediated by two major thalamic pathways, which signal light decrements (OFF) and increments (ON) in visual scenes, the OFF pathway being faster than the ON. Here, we demonstrate that this OFF temporal advantage is transferred to visual cortex and has a correlate in human perception. OFF-dominated cortical neurons in cats responded ~3 ms faster to visual stimuli than ON-dominated cortical neurons, and dark-mediated suppression in ON-dominated neurons peaked ~14 ms faster than light-mediated suppression in OFF-dominated neurons. Consistent with the neuronal differences, human observers were 6–14 ms faster at detecting darks than lights, and better at discriminating dark than light flickers. Neuronal and perceptual differences both vanished if backgrounds were biased towards darks. Our results suggest that the cortical OFF pathway is faster than the ON pathway at increasing and suppressing visual responses; and these differences have parallels in the human visual perception of lights and darks.

The specificity of cone inputs to ganglion cells has implications for the development of retinal connections and the nature of information transmitted to higher areas of the brain. We introduce a rapid and precise method for measuring signs and magnitudes of cone inputs to visual neurons. Colors of stimuli are modulated around circumferences of three color planes in clockwise and counterclockwise directions. For each neuron, the projection of the preferred vector in each plane was estimated by averaging the response phases to clockwise and counterclockwise modulation. The signs and weights of cone inputs were derived directly from the preferred vectors. The efficiency of the method enables us to measure cone inputs at different temporal frequencies and short-wavelength-sensitive (S) cone adaptation levels. The results show that S-cone inputs to the parvocellular and magnocellular ganglion cells are negligible, which implies underlying connectional specificity in the retinal circuitry.

Recent physiological studies claim that Dark stimuli have access to greater neuronal resources than Light stimuli in early visual pathway. We used two sets of novel stimuli to examine the functional consequences of this Dark dominance in human observers. We show that increment and decrement thresholds are equal when controlled for adaptation and eye-movements. However, measurements for salience differences at high-contrasts show that Darks are detected pronouncedly faster and more accurately than Lights when presented against uniform binary noise. In addition, the salience advantage for Darks is abolished when the background distribution is adjusted to control for the irradiation illusion. The threshold equality suggests that the highest sensitivities of neurons in the ON and OFF channels are similar, whereas the salience difference is consistent with a population advantage for the OFF system.

We have studied the responses of MT neurons to moving gratings, spatially modulated in luminance and chromaticity. Most MT neurons responded briskly and with high contrast sensitivity to targets whose luminance was modulated, with or without added chromatic contrast. When luminance modulation was removed and only chromatic stimulation was used, the responses of all MT neurons were attenuated. Most were completely unresponsive to stimulation with targets whose modulation fell within a "null" plane in color space; these null planes varied from neuron to neuron, but all lay close to the plane of constant photometric luminance. For about a third of the neurons, there was no color direction in which responses were completely abolished; almost all of these neurons had a definite minimum response for chromatic modulation near the isoluminant plane. MT neurons that responded to isoluminant targets did so inconsistently and with poor contrast sensitivity, so that only intensely modulated targets were effective. Whereas the best thresholds of MT neurons for luminance targets are close to behavioral contrast threshold, the thresholds for isoluminant targets lie considerably above behavioral contrast threshold. Therefore, although some MT neurons do give responses to isoluminant targets, they are unlikely to be the source of the chromatic motion signals revealed behaviorally.