Abstract

The howler monkeys (Alouatta sp.) are the only New World primates to exhibit routine trichromacy. Both males and females have three cone photopigments. However, in contrast to Old World monkeys, Alouatta has a locus control region upstream of each opsin gene on the X-chromosome and this might influence the retinal organization underlying its color vision. Post-mortem microspectrophotometry (MSP) was performed on the retinae of two male Alouatta to obtain rod and cone spectral sensitivities. The MSP data were consistent with only a single opsin being expressed in each cone and electrophysiological data were consistent with this primate expressing full trichromacy. To study the physiological organization of the retina underlying Alouatta trichromacy, we recorded from retinal ganglion cells of the same animals used for MSP measurements with a variety of achromatic and chromatic stimulus protocols. We found MC cells and PC cells in the Alouatta retina with similar properties to those previously found in the retina of other trichromatic primates. MC cells showed strong phasic responses to luminance changes and little response to chromatic pulses. PC cells showed strong tonic response to chromatic changes and small tonic response to luminance changes. Responses to other stimulus protocols (flicker photometry; changing the relative phase of red and green modulated lights; temporal modulation transfer functions) were also similar to those recorded in other trichromatic primates. MC cells also showed a pronounced frequency double response to chromatic modulation, and with luminance modulation response saturation accompanied by a phase advance between 10–20 Hz, characteristic of a contrast gain mechanism. This indicates a very similar retinal organization to Old-World monkeys. Cone-specific opsin expression in the presence of a locus control region for each opsin may call into question the hypothesis that this region exclusively controls opsin expression.

Highlights

  • In catarrhine primates (Old-World monkeys, apes, and humans), the genes for the middle- (M) and long-wavelength (L) sensitive opsins form a tandem array on the X chromosome and, together with the short-wavelength (S) cone opsin, coded on chromosome 7, form the basis for trichromacy [1,2,3]

  • In diurnal platyrrhine primates (New-World monkeys), usually only one longer wavelength opsin gene is found on the X chromosome but, depending of the species, two or more alleles are present [4], [5]

  • This means that all males are dichromats but if a female possesses two different alleles on her X chromosome pair, trichromatic color vision can be attained

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Summary

Introduction

In catarrhine primates (Old-World monkeys, apes, and humans), the genes for the middle- (M) and long-wavelength (L) sensitive opsins form a tandem array on the X chromosome and, together with the short-wavelength (S) cone opsin, coded on chromosome 7, form the basis for trichromacy [1,2,3]. In diurnal platyrrhine primates (New-World monkeys), usually only one longer wavelength opsin gene is found on the X chromosome but, depending of the species, two or more alleles are present [4], [5] This means that all males are dichromats but if a female possesses two different alleles on her X chromosome pair, trichromatic color vision can be attained. The Alouatta L- and M-photopigments have spectral absorption maxima at about 560 and 530 nm, close to those of catarrhines [12], but there may be some inter-individual variability [14] The genes coding these opsins are present in a tandem array on the X chromosome, as in catarrhines, but with a different structure [4], [14], [15]

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Conclusion

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