The primary visual cortex of carnivores and primates is dominated by the OFF visual pathway and responds more strongly to dark than light stimuli. Here, we demonstrate that this cortical OFF dominance is modulated by the size and spatial frequency of the stimulus in awake primates and we uncover a main neuronal mechanism underlying this modulation. We show that large grating patterns with low spatial frequencies drive five times more OFF-dominated than ON-dominated neurons, but this pronounced cortical OFF dominance is strongly reduced when the grating size decreases and the spatial frequency increases, as when the stimulus moves away from the observer. We demonstrate that the reduction in cortical OFF dominance is not caused by a selective reduction of visual responses in OFF-dominated neurons but by a change in the ON/OFF response balance of neurons with diverse receptive field properties that can be ON or OFF dominated, simple, or complex. We conclude that cortical OFF dominance is continuously adjusted by a neuronal mechanism that modulates ON/OFF response balance in multiple cortical neurons when the spatial properties of the visual stimulus change with viewing distance and/or optical blur.

Humans have been shown to rapidly detect animals in naturalistic scenes, but the role of color in this task is unclear. We first analyze the color information contained in a large number of images of salient and camouflaged animals in generic backgrounds. We found that color distributions of most animals and of their immediate backgrounds were oriented along other than the cardinal directions of color space. In addition, the maximum distances between animals and background distributions also tended to be along noncardinal directions, suggesting a role for higher-order cortical color mechanisms whose preferred axes are distributed widely in color space. We measured temporal thresholds for segmenting animal color distributions from background distributions in the absence of spatial cues. Combined over all observers and all images in our sample, thresholds for segmenting isoluminant projections of these distributions were lower than for segmenting the original distributions and considerably lower than for segmenting achromatic projections. Color information is thus likely to be useful in segregating animals in generic views, i.e., views not purposely chosen by the photographer to enhance the visibility of the animal. However, a comparison of thresholds with distances between distributions failed to reveal any advantage conferred by higher-order color mechanisms.

Local field potentials (LFPs) have become an important measure of neuronal population activity in the brain and could provide robust signals to guide the implant of visual cortical prosthesis in the future. However, it remains unclear whether LFPs can detect weak cortical responses (e.g., cortical responses to equiluminant color) and whether they have enough visual spatial resolution to distinguish different chromatic and achromatic stimulus patterns. By recording from awake behaving macaques in primary visual cortex, here we demonstrate that LFPs respond robustly to pure chromatic stimuli and exhibit ∼2.5 times lower spatial resolution for chromatic than achromatic stimulus patterns, a value that resembles the ratio of achromatic/chromatic resolution measured with psychophysical experiments in humans. We also show that, although the spatial resolution of LFP decays with visual eccentricity as is also the case for single neurons, LFPs have higher spatial resolution and show weaker response suppression to low spatial frequencies than spiking multiunit activity. These results indicate that LFP recordings are an excellent approach to measure spatial resolution from local populations of neurons in visual cortex including those responsive to color.

The unique hues--blue, green, yellow, red--form the fundamental dimensions of opponent-color theories, are considered universal across languages, and provide useful mental representations for structuring color percepts. However, there is no neural evidence for them from neurophysiology or low-level psychophysics. Tapping a higher prelinguistic perceptual level, we tested whether unique hues are particularly salient in search tasks. We found no advantage for unique hues over their nonunique complementary colors. However, yellowish targets were detected faster, more accurately, and with fewer saccades than their complementary bluish targets (including unique blue), while reddish-greenish pairs were not significantly different in salience. Similarly, local field potentials in primate V1 exhibited larger amplitudes and shorter latencies for yellowish versus bluish stimuli, whereas this effect was weaker for reddish versus greenish stimuli. Consequently, color salience is affected more by early neural response asymmetries than by any possible mental or neural representation of unique hues.

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.

Coloration and pattern are thought to play roles in crypsis for evading predators, and display for attracting mates or warning enemies. Colors of animals and their natural surroundings form distributions elongated between spectral reflectances and illumination spectra. We investigate whether color distributions contribute to camouflage and display independent of spatial information.We obtained 30 images of animals distinctly visible on the natural surround, and 29 images of animals camouflaged against their background. Colors were extracted from each pixel in the animal's image, and each pixel in the surrounding annulus of roughly the same width as the animal. The surround colors were randomly placed in the pixels of an 8 deg square, and the animal colors randomly in a 1.5 × 6 deg rectangle. Random masks were made as averages of all the images. Duration thresholds for discrimination of each animal color distribution from its background distribution, were measured by presenting rectangles randomly as horizontal or vertical in the center of the square, followed by a mask, in a 2AFC method of constant stimuli for durations from 8.5 to 100 msec. Besides the original distributions, the experiment also used isoluminant and achromatic versions of the random displays. Thresholds were determined from psychometric curves fitted to each image for each condition and for each observer. Comparing isoluminant thresholds to thresholds for the original distributions, reveals whether an animal distribution can be reliably detected on the basis of chromatic information alone. Comparing achromatic thresholds to thresholds for the original distributions reveals whether the addition of chromatic information enhances detection of an animal distribution. In general, both tests separated the images into the same groups, animals that could be detected using chromatic signals, and animals that could not. We will show that the usefulness of chromatic signals is related to the angular difference between color distributions.