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Color Vision Test for Dichromatic and Trichromatic Macaque Monkeys

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Color Vision Test for Dichromatic and Trichromatic Macaque Monkeys Journal of Vision (2013) 13(13):1, 1–15 http://www.journalofvision.org/content/13/13/1 1 Color vision test for dichromatic and trichromatic macaque monkeys National Institute for Physiological Sciences, Okazaki, Aichi, Japan Electronics-Inspired Interdisciplinary Research Institute, Toyohashi University of Technology, Toyohashi, Aichi, # Kowa Koida* Japan $ National Institute for Physiological Sciences, Okazaki, Aichi, Japan University for Advanced Studies (SOKENDAI), Okazaki, # Isao Yokoi* Aichi, Japan $ National Institute for Physiological Sciences, Okazaki, Aichi, Japan University for Advanced Studies (SOKENDAI), Okazaki, # Gouki Okazawa Aichi, Japan $ Faculty of Rehabilitation, Chubu Gakuin University, Seki, # Akichika Mikami Gifu, Japan $ Department of Biology, Bogor Agricultural University, # Kanthi Arum Widayati Bogor, Indonesia $ Primate Research Institute, Kyoto University, Inuyama, # Shigehiro Miyachi Aichi, Japan $ National Institute for Physiological Sciences, Okazaki, Aichi, Japan University for Advanced Studies (SOKENDAI), Okazaki, # Hidehiko Komatsu Aichi, Japan $ Dichromacy is a color vision defect in which one of the identified dichromatic macaques (Macaca fascicularis) three cone photoreceptors is absent. Individuals with with that of normal trichromatic macaques. In the color dichromacy are called dichromats (or sometimes ‘‘color- discrimination test, dichromats could not discriminate blind’’), and their color discrimination performance has colors along the protanopic confusion line, though contributed significantly to our understanding of color trichromats could. In the light detection test, the relative vision. Macaque monkeys, which normally have thresholds for longer wavelength light were higher in the trichromatic color vision that is nearly identical to dichromats than the trichromats, indicating dichromats humans, have been used extensively in to be less sensitive to longer wavelength light. Because neurophysiological studies of color vision. In the present the dichromatic macaque is very rare, the present study study we employed two tests, a pseudoisochromatic provides valuable new information on the color vision color discrimination test and a monochromatic light behavior of dichromatic macaques, which may be a detection test, to compare the color vision of genetically useful animal model of human dichromacy. The Citation: Koida, K., Yokoi, I., Okazawa, G., Mikami, A., Widayati, K. A., Miyachi, S., & Komatsu, H. (2013). Color vision test for dichromatic and trichomatic macaque monkeys. Journal of Vision, 13(13):1, 1–15, http://www.journalofvision.org/13/13/1, doi:10.1167/13.13.1. doi: 10.1167/13.13.1 Received May 3, 2013; published November 1, 2013 ISSN 1534-7362 Ó 2013 ARVO Downloaded from jov.arvojournals.org on 09/27/2021 Journal of Vision (2013) 13(13):1, 1–15 Koida et al. 2 behavioral tests used in the present study have been macaques, although macaque monkeys are widely previously used to characterize the color behaviors of used to study the neural mechanisms of color vision trichromatic as well as dichromatic new world monkeys. (Gegenfurtner, 2003; Komatsu, 1998; Solomon & The present results show that comparative studies of Lennie, 2007). color vision employing similar tests may be feasible to Macaque monkeys have trichromatic color vision examine the difference in color behaviors between homologous to that in humans (De Valois, Morgan, trichromatic and dichromatic individuals, although the Polson, Mead, & Hull, 1974; Oyama, Furusaka, & genetic mechanisms of trichromacy/dichromacy is quite Kito, 1986; Stoughton et al., 2012). However, through different between new world monkeys and macaques. molecular genetic analysis we demonstrated the existence of a dichromatic genotype among the crab- eating macaques (Onishi et al., 1999). Using poly- Introduction merase chain reaction (PCR) to specify genotype, we identified male dichromats and female heterozygotes spread among some troops in Pangandaran National Color vision has been studied in a wide range of Park, Indonesia. Moreover, absorbance spectrum animal species. These studies have established the analysis of their photoreceptors (Onishi et al., 1999) presence or absence of color vision as well as the and spectral sensitivity measurements using electro- dimensionality and sharpness of color vision in retinogram flicker photometry (Hanazawa et al., 2001) different species (Jacobs, 2009, 2012; Jacobs & Nathans, 2009; Mancuso, Neitz, & Neitz, 2006). They revealed that those animals lack the L photopigment have also provided fundamental knowledge that has (protanopic dichromats). increased our understanding of the function of color In the present study, we examined the color vision vision and its biological basis. Among the various of dichromatic and trichromatic macaques using two species studied, monkeys are in close lineage to behavioral tests related to the two symptoms of humans, so an understanding of color vision in human protanopic dichromats. We first conducted a monkeysisofparticularrelevancefortheunder- pseudoisochromatic test to examine the ability of standing of color vision in humans. macaques to discriminate a colored target from Color vision of primates have been studied using achromatic distracters. In the second test, the spectral various behavioral tests including measurement of sensitivities to two monochromatic lights were com- increment-threshold spectral sensitivity (Blakeslee & pared to assess the sensitivity to long wavelength light. Jacobs, 1982; Jacobs, 1972, 1977, 1983, 1984; Jacobs Both of these methods have been used previously to & Blakeslee, 1984; Sidley & Sperling, 1967), wave- examine the color vision of monkeys. Spectral length discrimination (Blakeslee & Jacobs, 1982; De sensitivities have been measured for a long time Valois & Morgan, 1974; Jacobs, 1984; Mollon, (Jacobs, 1972; Sidley & Sperling, 1967), and pseudo- Bowmaker,&Jacobs,1984),Rayleighmatch(Blakes- isochromatic tests have been more recently applied to lee & Jacobs, 1982; Jacobs, 1984; Mollon et al., 1984; cathode ray tube (CRT) display (Reffin, Astell, & Blakeslee & Jacobs, 1985), or a pseudoisochromatic Mollon, 1991; Regan, Reffin, & Mollon, 1994), and test (Mancuso, Hauswirth et al., 2009; Mancuso, they were used to characterize the color discrimination Neitz et al., 2006; Saito, Kawamura et al., 2005; abilities of squirrel monkeys whose color vision was Saito, Mikami et al., 2003), and these studies have genetically identified (Mancuso, Hauswirth et al., characterized the properties of color vision of various 2009; Mancuso, Neitz et al., 2006). Our present study primate species. These behavioral studies have shown will contribute in two aspects to that body of the presence of polymorphisms in color vision within knowledge. First, although it is known that both a number of species in new world monkeys, and trichromatic and dichromatic individuals exist among color vision behaviors were compared between various new world monkey species, their genetic trichromatic and dichromatic individuals (Blakeslee mechanisms of trichromacy/dichromacy are very & Jacobs, 1982; Jacobs, 1977, 1983, 1984, 1990; different from those in old world primates, including Jacobs & Blakeslee, 1984; Jacobs, Neitz, & Crognale, macaques and humans (Jacobs, 1998, 2008; Jacobs & 1987; Mollon et al., 1984). These observations and Nathans, 2009; Nathans, 1999). Therefore, the di- the estimated underlying mechanisms were consistent chromatic macaque may be a more appropriate with the results from genetic analysis or the analyses animal model with which to conduct studies to based on physiological methods such as microspec- investigate the neural mechanisms underlying human tro-photometric measurement or electroretinogram color vision, and the present study is the first attempt (Bowmaker, Jacobs, & Mollon, 1987; Jacobs, Bow- to examine the color discrimination behavior of maker, & Mollon, 1981; Jacobs et al., 1987). dichromatic macaques. Second, the frequency of However, no study has yet compared color vision dichromacy in macaques is very low: Dichromatic behaviors between trichromatic and dichromatic macaques have been found in only one place so far. Downloaded from jov.arvojournals.org on 09/27/2021 Journal of Vision (2013) 13(13):1, 1–15 Koida et al. 3 Consequently, this strain could be very useful for nated experimental cage (W50 · D40 · H70 cm), studying the development and neurophysiology of after which the experimenter started the task control neural circuits for color vision in macaques. It is program. Three images, one target, and two distrac- therefore of importance to characterize the color tors (4.5 cm · 4.5 cm each, Figure 1a), were then vision behavior of these animals. presented on a computer screen (FlexScan EV2335W, NANAO, Epson, Matsumoto, Japan) located on a wall of the experiment cage (Figure 1b). The pixel size on the screen was 0.265 mm, and size of each image Materials and methods was 170 · 170 pixels. Both the target and the distractors appeared on a black background. Below Animals each image, there was a button, and the monkey was rewarded with a small piece of sweet potato or apple if Two genetically identified dichromatic (males 4.5–5.0 it pressed the button below the target image. The kg; Didi, Dito) and two normal trichromatic (one animal was allowed to press the button while the female and one male 2.7–5.8 kg; Nofy, Noby) crab- stimuli were presented (2.0–2.6 s), and after a button eating macaques (Macaca fascicularis) participated in was pressed all three
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