Color-hierarchies in executive control of monkeys' behavior.

Processing advantages for particular colors (color-hierarchies) influence emotional regulation and cognitive functions in humans and manifest as an advantage of the red color, compared with the green color, in triggering response inhibition but not in response execution. It remains unknown how such color-hierarchies emerge in human cognition and whether they are the unique properties of human brain with advanced trichromatic vision. Dominant models propose that color-hierarchies are formed as experience-dependent learning that associates various colors with different human-made conventions and concepts (e.g., traffic lights). We hypothesized that if color-hierarchies modulate cognitive functions in trichromatic nonhuman primates, it would indicate a preserved neurobiological basis for such color-hierarchies. We trained six macaque monkeys to perform cognitive tasks that required behavioral control based on colored cues. Color-hierarchies significantly influenced monkeys' behavior and appeared as an advantage of the red color, compared to the green, in triggering response inhibition but not response execution. For all monkeys, the order of color-hierarchies, in response inhibition and also execution, was similar to that in humans. In addition, the cognitive effects of color-hierarchies were not limited to the trial in which the colored cues were encountered but also persisted in the following trials in which there was no colored cue on the visual scene. These findings suggest that color-hierarchies are not resulting from association of colors with human-made conventions and that simple processing advantage in retina or early visual pathways does not explain the cognitive effects of color-hierarchies. The discovery of color-hierarchies in cognitive repertoire of monkeys indicates that although the evolution of humans and monkeys diverged in about 25 million years ago, the color-hierarchies are evolutionary preserved, with the same order, in trichromatic primates and exert overarching effects on the executive control of behavior.

Perceptual Color Space Representations in the Oculomotor System Are Modulated by Surround Suppression and Biased Selection.

The oculomotor system utilizes color extensively for planning saccades. Therefore, we examined how the oculomotor system actually encodes color and several factors that modulate these representations: attention-based surround suppression and inherent biases in selecting and encoding color categories. We measured saccade trajectories while human participants performed a memory-guided saccade task with color targets and distractors and examined whether oculomotor target selection processing was functionally related to the CIE (x,y) color space distances between color stimuli and whether there were hierarchical differences between color categories in the strength and speed of encoding potential saccade goals. We observed that saccade planning was modulated by the CIE (x,y) distances between stimuli thus demonstrating that color is encoded in perceptual color space by the oculomotor system. Furthermore, these representations were modulated by (1) cueing attention to a particular color thereby eliciting surround suppression in oculomotor color space and (2) inherent selection and encoding biases based on color category independent of cueing and perceptual discriminability. Since surround suppression emerges from recurrent feedback attenuation of sensory projections, observing oculomotor surround suppression suggested that oculomotor encoding of behavioral relevance results from integrating sensory and cognitive signals that are pre-attenuated based on task demands and that the oculomotor system therefore does not functionally contribute to this process. Second, although perceptual discriminability did partially account for oculomotor processing differences between color categories, we also observed preferential processing of the red color category across various behavioral metrics. This is consistent with numerous previous studies and could not be simply explained by perceptual discriminability. Since we utilized a memory-guided saccade task, this indicates that the biased processing of the red color category does not rely on sustained sensory input and must therefore involve cortical areas associated with the highest levels of visual processing involved in visual working memory.