If, years later, students remember anything from their first exposure to the study of the eye, it is that rods allow you to see at night while cones fulfill a similar role during the daytime. In retrieving this nugget of wisdom, they carry forward a principal tenet of duplicity theory, one of the earliest and most enduring generalizations in the study of sight. While there is little argument that duplicity theory constitutes an important chapter in the history of vision science, references to it have disappeared from the contemporary research literature. So is duplicity theory just another dusty chapter, now supplanted by the emergence of detailed understanding of the issues it was designed to encompass? Bjorn and Ulf Stabell think not and have produced this concise and gracefully written book to document their argument.
The book contains, as the title advertises, a history of the development and evaluation of duplicity theory over the years. The authors discern the roots of the theory as extending all the way to writings of the ancient Greeks, who as early as the fifth century BCE hypothesized that variations among species in their abilities to see by day and by night might be explained as due to differences in the respective amounts of two elements (“fire” and “water”) found in their inner eyes. But of course for most the theory was initiated by the work of the anatomist Max Schultze, who in 1866 published observations on the retinal anatomy of eyes for many different species. From these, he was led him to believe cones were absent from the retinas of various nocturnal animals, rods from those of some diurnal animals, and, given that, it was logical to link rods to night vision and cones to daylight vision and to infer that cones must mediate characteristic features of daylight vision, including fine spatial discrimination and color vision. By the time Schultze’s work appeared discussions about evolution were in the air, and it is notable that he believed that rods were the more primitive of the receptor types with cones and the functional consequences their presence carries constituting a more derived development. In the years immediately following Schultze’s publication, Boll, Kΰhne, and König all carried out ground-breaking studies that linked photopigment properties to dark adaptation and to spectral sensitivity, thus providing crucial biochemical links between structure and function. It was then left to von Kries who starting in 1894 and continuing forward for about the next three decades drew these various pieces of evidence together and provided the designation “duplicity theory.” According to the authors, by the early 20th century, the theory had become generally accepted.
But even if duplicity theory had reached the mainstream by that point, there were still plenty of issues requiring resolution. Central among these was to understand how contributions from rods and cones got translated into sight. Physiology was still too primitive to be of much help here so the early advances mostly emerged out of what the authors identify as the tradition established by Goethe. Core to this approach were explorations of the phenomenology of color appearance, the most celebrated contributed by Ewald Hering who drew attention to the fact that color appearance, as well as a range of contrast and induction effects, was best explained by assuming the presence in the visual system of antagonistic (opponent) processes. Followers of Hering, including prominently G. E. Müller, offered sophisticated theories of color vision based on opponent processes. Yet despite many early demonstrations of the roles that both excitation and inhibition play in the nervous system, the more hard-minded of the vision establishment resisted the idea that combined excitatory and inhibitory effects played a central role in the analysis of visual information. As the authors document, this began to change about 1940, with the advent of the ability to record from single nerve cells and the subsequent direct demonstration from this approach of the interplay of excitation and inhibition, first in the domain of spatial coding and then later through the discovery of spectrally opponent units in a wide variety of different species that illustrated the nature of combination for signals derived from different classes of cone.
In an influential review that stands as a clear predecessor to this book, Saugstad and Saugstad (Reference Saugstad, Saugstad and Streiff1959) interpreted classic duplicity theory as proposed by Schultze to mean that rods and cones operated in total independence of one another. The book reviews the wealth of subsequent data derived from anatomy, physiology, and psychophysics that demonstrates to the contrary. Early in the course of these studies, for example, it became clear why rods, although more densely packed than cones, only supported much coarser spatial resolution and that cones and rods shared common neural pathways, thus providing potential anatomical substrates for their interactions. The issue of rod/cone independence has been especially pursued in the context of rod contributions to color vision. The large (and to this outsider somewhat confusing) literature on this is covered in detail by the authors, themselves central contributors to this topic.
The latter part of the book contains a summary of more recent advances, bringing the story of duplicity theory forward to the present. The work covered mostly ends some years ago and that may seem a bit disappointing because signal advances continue to be made on topics that were central to duplicity theory. Among these, for example, (1) evidence derived from comparative analysis of opsin genes shows that in the evolution of eyes, cones emerged well before rods made their appearance, a reversal of the idea originated by Schultze and then carried forward for many years; (2) the processes that underlie relatively rapid change in rod/cone proportions thus equipping animals to adaptively migrate along the duplicity dimension are being unveiled; and (3) many of the essential differences between rod and cone responses (sensitivity and response kinetics) are now traced downward to differences in the proteins involved in phototransduction. This small quibble aside, the authors have produced a nice account of duplicity theory that will be of interest to those vision scientists who wish to better understand how we got to where we are today.