Experimental evidence that primate trichromacy is well suited for detecting primate social colour signals

Abstract

Primate trichromatic colour vision has been hypothesized to be well tuned for detecting variation in facial coloration, which could be due to selection on either signal wavelengths or the sensitivities of the photoreceptors themselves. We provide one of the first empirical tests of this idea by asking whether, when compared with other visual systems, the information obtained through primate trichromatic vision confers an improved ability to detect the changes in facial colour that female macaque monkeys exhibit when they are proceptive. We presented pairs of digital images of faces of the same monkey to human observers and asked them to select the proceptive face. We tested images that simulated what would be seen by common catarrhine trichromatic vision, two additional trichromatic conditions and three dichromatic conditions. Performance under conditions of common catarrhine trichromacy, and trichromacy with narrowly separated LM cone pigments (common in female platyrrhines), was better than for evenly spaced trichromacy or for any of the dichromatic conditions. These results suggest that primate trichromatic colour vision confers excellent ability to detect meaningful variation in primate face colour. This is consistent with the hypothesis that social information detection has acted on either primate signal spectral reflectance or photoreceptor spectral tuning, or both.

Color tuning of neurons in face patches of macaque inferior temporal cortex

“…In a second series of experiments, we found that face-selective cells were not very responsive to pure color (equiluminant) images of faces, but nonetheless maintained a bias for L>M. The results confirm prior results showing the importance of luminance contrast for face selectivity (Ohayon et al, 2012), and provide single-unit evidence supporting the fMRI observation that face patches respond more strongly to luminance contrast compared to equiluminant color (Lafer-Sousa and Conway, 2013). We speculate that the prior for L>M colors reflects the role of face color as a cue in trichromatic primates, in both humans and macaque monkeys, to sex, dominance, health, and emotion (Conway, 2018;Dubuc et al, 2009;Hiramatsu et al, 2017;Setchell and Wickings, 2005;Stephen et al, 2009;Waitt et al, 2003). The present results uncovering a neural implementation for this prior could provide clues to the neural mechanisms that support these important behaviors.…”

“…We might therefore expect an agreement between neural tuning and the statistics of those parts of the environment that are behaviorally relevant (Wei and Stocker, 2015). Face color is important for behavior in trichromatic primates, providing a cue to sex, dominance, health, and emotion (Waitt et al, 2003;Setchell and Wickings, 2005;Dubuc et al, 2009;Stephen et al, 2009;Hiramatsu et al, 2017;Conway, 2018). Moreover, faces occupy a distinct gamut in color space (Crichton et al, 2012;Chauhan et al, 2015), in which the dynamic color component is determined predominantly by hemoglobin oxygenation (this is true for people regardless of race, as well as in non-human primates that have lost some facial hair such as macaque monkeys).…”

Untitled

“…Fourth and finally, we had no behavioural data to show that males are 281 directly responsive to changes in skin temperature, and can be deceived by pregnant females who 282 may have similar skin temperature profiles as fertile individuals. Nevertheless, we consider this a 283 likely possibility, mainly because shifts in blood flow, and their corresponding changes in skin 284 temperature, may affect skin colouration in the face and elsewhere, which can be perceived by 285 recipients (Hiramatsu et al 2017). 286 In sum, our data appear consistent with the prediction that, during gestation, chimpanzee females 287 not only approximate behavioural and visual cues that characterise non-pregnant females, but 288 also physiological cues.…”

Platyrrhine color signals: New horizons to pursue

“…Simulated appearance of a female rhesus macaque ( Macaca mulatta ; Cayo Santiago) for: a trichromatic observer (a); a dichromatic observer (b) . Peak cone sensitivity values on simulations of trichromatic Rhesus macaque vision (S cone = 420 nm; M cone = 530 nm; L cone = 560 nm) and a protanomalous dichromatic type (S cone = 420 nm; M cone = 530 nm) . Photo by ADM…”

“…80 Peak cone sensitivity values on simulations of trichromatic Rhesus macaque vision (S cone = 420 nm; M cone = 530 nm; L cone = 560 nm) and a protanomalous dichromatic type (S cone = 420 nm; M cone = 530 nm). 45 Photo by ADM…”