Part IV  Theories of sensitivity regulation of the rod and cone systems: a historical account

15  Introduction

The most basic assumption of the orthodox duplicity theory that only rods function in night vision and only cones in day vision has been generally agreed on during the whole developmental period from Schultze (1866) to the present (2009).

Schultze had provided two strong arguments in favour of this basic assumption. Firstly, rods and cones tended to dominate innocturnal and diurnal species, respectively. In fact, some nocturnal species had a pure rod and some diurnal species a pure cone retina.Secondly, colour vision, a characteristic feature of cones of the central fovea, was absent in night vision.

Reasoning from this assumption, one would expect that a reduction in light intensity from that of daylight would lead to the functional appearance of rods at some particular intensity level. Schultze, however, did not state where and how this transition from cone to rod vision and vice versa happened. Furthermore, he did not provide any theory to explain the difference in sensitivity between the two receptor types. This reveals a serious limitation in his theory construction and shows that the most basic assumption of his theory was without any adequate explanation.

Several of the leading scientists within vision research have attempted to bridge this gap in Schultze’s theory construction by developing theories of the sensitivity regulation mechanisms of the rod and cone receptor systems. Actually, the development of these theories may be considered a main thread in the history of the duplicity theory. The theories offered by Hecht, Wald, Rushton, Barlow and Lamb dominated the scene and will all be dealt with in some detail.

16  Early photochemical explanations

A first clue to an understanding of the sensitivity regulation mechanism in rods was given by the discovery by Boll in 1876 that the photopigment rhodopsin, situated in the outer segment of the rod receptors, was bleached by light and regenerated in the dark. He also showed that the bleaching effect of light depended on the wavelength used (Boll, 1878).

Influenced by this great discovery, Kühne, in an extensive research work, provided strong evidence in favour of the view that the sensitivity difference between rods and cones had a ­photochemical basis (Kühne, 1877a, b, 1877–1878, 1879). He investigated the bleaching and regeneration processes of rhodopsin in much more detail than Boll and made an important theoretical contribution with his influential ‘Optochemische’ hypothesis, where he presumed that the phototransduction in both rods and cones was photochemical in nature. Accordingly, he presumed that the apparent colourless cone receptors contained photochemical substances, and that these substances became involved in visual processing under daylight conditions. Indeed, in opposition to Schultze’s (1866) duplicity theory, he presumed that even rods were activated by photochemical, colourless substances in daylight.

Furthermore, Kühne (1879) made an important distinction between the photochemical substances and their photoproducts, and argued that it was the photoproducts, not the photosensitive substances that generated the neural activity in the retina. Moreover, he discovered that rhodopsin may regenerate in two quite different ways: a rapid anagenese from photoproducts of rhodopsin and a slower neogenese from new substances formed after rhodopsin had been bleached. The relative contribution of these two processes was

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assumed to determine the speed of recovery of the rhodopsin pigment in the dark and, hence, the speed of the dark-adaptation process. Consequently, he suggested that dark adaptation would proceed most slowly when all rhodopsin molecules had been bleached.

The hypothesis that the photopigment rhodopsin could account for the sensitivity difference between rods and cones was apparently first unequivocally put forward by Parinaud (1885). He had found that ‘hèmèralopie’ reduced the sensitivity of the eye markedly and attributed this sensitivity reduction to the non-functioning of rhodopsin. In fact, he held that only the rod receptors had the ability to increase their sensitivity during dark adaptation and that the amount of rhodopsin determined the variation in sensitivity of the eye both during light and dark adaptation. He found confirming evidence in that the central fovea, which contained only cones, did not function in night vision, and that the photochromatic interval (the intensity interval between absolute light and chromatic thresholds) was nearly absent in the central fovea.

The final conclusive proof that the photopigment rhodopsin in the rods was responsible for night vision was given a few years later by König (1894) who showed that the spectral absorption of rhodopsin in humans closely coincided with the scotopic spectral visibility curve.

However, the suggestion of Parinaud that only the rods had the capacity to increase their sensitivity during dark adaptation was found to be wrong. Thus, Loeser (1904) convincingly demonstrated that the cones also had the ability to adapt to darkness. In fact, following strong bleaches he found that cones could improve their sensitivity by more than 1 log unit during the first few minutes of dark adaptation.