The two subsystems of colour vision and their roles in wavelength discrimination

Horace Barlow makes only occasional forays into the field of colour vision (Barlow, 1958,1982), but when he does, he always leaves us with much to think about. In his 1982 paper 'What causes trichromacy? ', he gave us a novel way of considering the information content of a coloured spectrum: he expressed the detailed structure of the colour spectrum in terms of its Fourier components and he treated the three photopigments (Fig. 11.1) as low-pass filters that would differentially attenuate the different Fourier components. Owing to the broad bandwidth of the filters, the visual system is insensitive to the fine structure of the colour spectrum; that is to say, if the amplitude of a stimulus varies periodically with wavelength and if the period of this modulation is small, then the response of the visual system will show little variation as the phase of the modulation is changed (Barlow, 1982). In considering his main question that of why our colour vision is three-dimensional Barlow was led also to ask several secondary questions: 'Why do the photopigments have such broad bandwidths? ', Are broad bandwidths deleterious to hue discrimination? ' and 'Why are the peak sensitivities of the pigments so asymmetrically placed in the spectrum? ' We hope that the present paper may say something in answer to these secondary questions. We first put forward a general view of the early stages of colour vision, the view that it consists of two subsystems, one recently overlaid on a much earlier one; and then we review some experimental work on wavelength discrimination, work that bears on the two subsystems of colour vision. The emerging view of colour vision is one that has long been suggested by the distribution of colour discrimination among the mammals (Jacobs, 1982); by the relative incidences of different forms of colour blindness in man (Ladd-Franklin, 1892); and by a number of asymmetric features of our colour vision, such as the relative paucity of the short-wave receptors (compared with the middleand long-wave receptors) and indeed the asymmetric arrangement of the absorbance curves of the photopigments (Gouras, 1984; Mollon, 1986; Mollon & Jordan, in press). It is a view consistent with Derrington, Krauskopf & Lennie's electrophysiological analysis of the parvocellular layers of the lateral geniculate nucleus (Derrington et al., 1984). But, above all, it is a view prompted by the molecular biology of the visual pigments published by Nathans and his collaborators (Nathans et al., 1986a,b). The most salient -findings of Nathans et al. are: first, that the genes for the longand middle-wave pigments lie very close together on the q-arm of the Xchromosome, and second, that the amino-acid sequences for the two pigments are 96% identical. It appears that visual pigments all consist of seven helices, which span the membrane and form a palisade surrounding the retinal, the prosthetic group that gives the pigment its spectral sensitivity (Fig. 11.2). The solid circles in the diagram to the bottom right of Fig. 11.2 show the small number of amino acids that Nathans et al. identify as different between the longand middle-wave pigments. The strong implication is that these two pigments were differentiated only very recently,' by duplication of an ancestral gene. On the