Psychophysical Chromatic Mechanisms in Macaque Monkey

Abstract

Chromatic mechanisms have been studied extensively with psychophysical techniques in humans, but the number and nature of the mechanisms are still controversial. Appeals to monkey neurophysiology are often used to sort out the competing claims and to test hypotheses arising from the experiments in humans, but psychophysical chromatic mechanisms have never been assessed in monkeys. Here we address this issue by measuring color-detection thresholds in monkeys before and after chromatic adaptation, employing a standard approach used to determine chromatic mechanisms in humans. We conducted separate experiments using adaptation configured as either flickering full-field colors or heterochromatic gratings. Full-field colors would favor activity within the visual system at or before the arrival of retinal signals to V1, before the spatialtransformationofcolorsignalsbythecortex.Conversely,gratingswouldfavoractivitywithinthecortexwhereneuronsareoftensensitive tospatialchromaticstructure.Detectionthresholdswereselectivelyelevatedforthecolorsoffull-fieldadaptationwhenitmodulatedalongeither of the two cardinal chromatic axes that define cone-opponent color space [L vs M or S vs (L ϩ M)], providing evidence for two privileged cardinal chromatic mechanisms implemented early in the visual-processing hierarchy. Adaptation with gratings produced elevated thresholds for colors of the adaptation regardless of its chromatic makeup, suggesting a cortical representation comprised of multiple higher-order mechanisms each selective for a different direction in color space. The results suggest that color is represented by two cardinal channels early in the processing hierarchy and many chromatic channels in brain regions closer to perceptual readout.

Color-detection thresholds in rhesus macaque monkeys and humans

“…Informed consent was obtained from human participants. Three adult male rhesus macaque monkeys (Macaca mulatta) and four female human subjects with normal trichromatic vision (tested with Ishihara plates) were trained to perform a color-detection task ( Figure 1A) using standard behavioral training techniques (Stoughton et al, 2012). Detection thresholds were measured using stimuli defined by the cone-opponent coordinates with which the retina encodes color (Derrington, Krauskopf, & Lennie, 1984;Hansen & Gegenfurtner, 2006;MacLeod & Boynton, 1979).…”

“…Weber cone contrasts shown in Figure 1 were obtained by taking the dot product of the spectral power distribution for stimuli and the cone fundamentals (Smith & Pokorny, 1972, 1975. The task design was similar to that described by Stoughton et al (2012), with the exception that stimuli used presently were embedded in luminance noise, and all trials were performed under constant neutral adaptation.…”

“…Subjects showed no obvious bias in target location (Figure 1B,right). Headposts were secured to the animals' skulls (Stoughton et al, 2012) to enable head fixation, which allowed for accurate eyemovement monitoring. Human subjects used a chin rest.…”

“…The most widely cited comparative work, conducted over 35 years ago, concluded that macaque monkeys have excellent color vision that is probably on par with that of humans (De Valois, Morgan, Polson, Mead, & Hull, 1974;Sidley et al, 1965). Consistent with this conclusion, monkeys have similar higher order psychophysical chromatic mechanisms to those documented in humans (Stoughton, Lafer-Sousa, Gagin, & Conway, 2012). But direct comparisons of absolute chromatic detection have not been performed with controlled viewing and equiluminant stimuli; most previous comparative work has focused instead on the shape of spectral sensitivity functions (Harwerth & Smith, 1985).…”

Colour vision in mantis shrimps: understanding one of the most complex visual systems in the world

“…On the basis of physiological and anatomical research in macaque monkeys, a trichromat with color vision very similar to humans (Stoughton, Lafer-Sousa, Gagin, & Conway, 2012), we have reason to believe that the computations carried out by the colorvision systems in humans and mantis shrimp are more similar than they first appear. Although color in trichromatic primates is encoded using three (not 12) classes of broadly tuned photoreceptors, primates have much larger brains than shrimp: neural circuits compare cone responses within the retina (Sun, Smithson, Zaidi, & Lee 2006), and the neural circuits responsible for color perception are linked across several different cortical regions .…”