23  Rushton and Barlow compared

As can be seen, the theories of light and dark adaptation proposed by Rushton and Barlow disagreed both with regard to the site of the gain-determining mechanisms and the question of whether light and dark adaptation were equivalent.

In the 1965 version, Rushton held that the two processes were controlled in an AGC pool located centrally to the photoreceptors, while in the 1972 version he suggested that dark adaptation mainly occurred in the receptors and light adaptation in horizontal cells. In both versions he held that light and dark adaptation were quite different processes.

The noise theory of Barlow, on the other hand, presumed that lightand dark-adaptation processes were equivalent and located mainly in the receptors – that light adaptation mainly resulted fromstatistical fluctuation of photons of the background light, while dark adaptation was controlled by photon-like events, possibly originating from photoproducts as a stream of events fluctuating randomly like the photons.

24  The Dowling-Rushton

equation refuted

24.1  Contribution of T.D. Lamb

The theories of Rushton and Barlow were very much alive in the 1960s and 1970s and dominated the discussion about visual adaptation. The most convincing defence of Barlow’s view was published by Lamb (1981). He admitted that Rushton’s theory had received stronger support from the scientific community, but argued that Barlow’s theory could more easily be reconciled with known properties of the visual system. He supported his view by presenting three strong arguments against Rushton’s theory: (1) intracellular electrical recording from rods and cones under conditions of light adaptation had shown that photoreceptors could become desensitized in a way approximating the Weber law, (2) Rushton’s theory implied that the photoreceptor could generate two quite different signals: an incident light intensity signal and a signal of the fraction of bleached photopigment, but no distinguishing mechanism located in the receptor had been found, and (3) the uniform desensitizing effect found by Rushton and Westheimer (1962) and Rushton (1965a) could not be repeated in an experiment performed by Barlow and Andrews (1973). In fact, these authors found a marked difference between sensitivity in the dark and bleached areas.

Lamb (1981) then went on to propose his own specification of Barlow’s theory. By analyzing a series of rod dark-adaptation curves of a trichromat previously published by Pugh (1975), he came to the conclusion that the long-term dark-adaptation curve of rods could best be described by three straight lines, each with a different slope. Furthermore, he suggested that these three different segments of the rod dark-adaptation curve were determined by the decay of three photochemical products S1, S2 and S3. Indeed, he proposed a

176theories of sensitivity regulation

direct proportionality between threshold elevation and photoproduct concentration and, hence, suggested that the three different segments of the rod dark-adaptation curve were direct plots of the decay of the three photochemical products.

To account for the threshold elevation effect of the photoproducts, he presumed that they produced ‘dark light’ or ‘noise’ like a stream of photon events. Specifically, he held that the formation

of a hypothetical photoproduct and activator S0 determined the ­transduction process in the same way irrespective of whether S0 was produced by photoisomerization, thermalisomerization, or by reverse

biochemical reactions from the three intermediates S1, S2 and S3.

In addition to the psychophysical evidence, Lamb (1981) could provide strong electrophysiological evidence in support of his theory. Thus, he had observed an increased fluctuation in the rod outersegment current following a bleach. Indeed, the fluctuation had the form expected for randomly occurring photon-like events.

It should be noted that the photoproducts S0, S1, S2 and S3 are hypothetical constructs. The model as it stands, therefore, faces the problem of identifying and measuring the concentration of the four substances during rod dark adaptation and also of providing

evidence that S1, S2 and S3, in fact, are responsible for the three components of desensitization found in the rod dark-adaptation curves.

Yet, if correct, the theory of Lamb would provide an ingenious solution to Rushton’s major problem of finding an explanation of the Dowling-Rushton equation. This equation had become generally accepted in the 1960s and 1970s, but since it required that the reduction in sensitivity was exponentially related to the fraction of pigment still bleached (log T = cB, i.e. T = 10cB), it could not be interpreted on a molecular level. Rushton et al. (1969, p. 473), therefore, had to admit, ‘The threshold is raised very greatly by bleaching – in rods by about 1 log unit for each 5% of rhodopsin bleached – and we understand neither the mechanism nor the meaning.’

the dowling-rushton equation refuted 177

As we have seen, Lamb’s (1981) solution to this problem was to suggest that the long-term rod dark-adaptation curve consisted of three different segments, each with a different slope, and that these three different slopes were direct plots of the decay of three different photoproducts.

Strong support of Lamb’s assumption that the long-term rod dark-adaptation curve is best described by different consecutive segments was provided by Nordby et al. (1984) and Stabell et al. (1986b). Using a complete rod monochromat (K. N.) as subject, these authors could measure the sensitivity increase of the rod system during dark adaptation for about 7 log units and found, unexpectedly, that a major, middle part of the curve closely followed a straight line with a slope that was independent of size, exposure time and retinal location of the test stimulus.

Similar results were also obtained with trichromats (Stabell­ et al., ­1986a). The slope of the straight line component was found to be remarkably constant, not only in a given individual, but in different individuals as well. Hence, the evidence appeared to support the notion of Lamb (1981, 1990) that the normal long-term rod dark-adaptation curve consisted of several segments each with its own underlying mechanism.

24.2  The search for a new formula

The obvious next step was to relate the sensitivity change obtained during the middle, straight line part of the long-term rod dark- ­adaptation curve to concomitant change in amount of bleached rhodopsin (see Boll, 1877; Parinaud, 1885; Hecht, 1921/1922; Wald, 1954; Dowling, 1960; Barlow, 1964; Rushton, 1965a; Lamb, 1981; Pepperberg, 1984). By relating the psychophysical data of the rod monochromat and the trichromats to previous measurements of rhodopsin regeneration (Rushton & Powell, 1972b), a formula quite different from the Dowling-Rushton equation emerged. Thus, the results suggested that for both rod monochromats and normal trichromats the relationship between threshold elevation T and