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Evolution of the Circuitry for Conscious Color Vision in Primates J Neitz and M Neitz 287 Eye (2017) 31, 286–300 © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved 0950-222X/17 www.nature.com/eye RCOPHTH EPONYMOUS LECTURE Evolution of the J Neitz and M Neitz circuitry for conscious color vision in primates Abstract Introduction There are many ganglion cell types and Color is the perception associated with the subtypes in our retina that carry color spectral composition of light. The question information. These have appeared at different addressed here is what is the circuitry times over the history of the evolution of the responsible for conscious color 'perception'. vertebrate visual system. They project to We are concerned with the neural machinery several different places in the brain and serve responsible for the hues, red, green blue and a variety of purposes allowing wavelength yellow, and how they are separated from black information to contribute to diverse visual and white. Countless ideas have been proposed functions. These include circadian relating to the neural underpinnings for human photoentrainment, regulation of sleep and color perception. The goal here is not to add mood, guidance of orienting movements, new ideas, but rather to examine evidence from detection and segmentation of objects. Predecessors to some of the circuits serving experiments in combination with consideration these purposes presumably arose before of constraints from evolution to determine mammals evolved and different functions are which ideas are most likely to be true. From represented by distinct ganglion cell types. those we attempt to synthesize the best possible However, while other animals use color current explanation of the physiological information to elicit motor movements and mechanisms underlying human color regulate activity rhythms, as do humans, perception. Department of using phylogenetically ancient circuitry, the Understanding the circuitry for color vision is Ophthalmology, School of ability to appreciate color appearance may important because it helps explain our conscious Medicine, Vision Sciences have been refined in ancestors to primates, and unconscious reactions to colored stimuli. It at South Lake Union/ mediated by a special set of ganglion cells can also explain the remarkable agreement Ophthalmology, University of Washington, Seattle, that serve only that purpose. Understanding across people about the appearance of some WA, USA the circuitry for color vision has implications colors in the face of differences in our physiology for the possibility of treating color blindness and the exceptional disagreement we have about Correspondence: using gene therapy by recapitulating other colors. In addition, we can better J Neitz, Department of evolution. In addition, understanding how understand how color vision deficiencies differ Ophthalmology, School of color is encoded, including how chromatic Medicine, Vision Sciences at from normal vision and consider the prospects and achromatic percepts are separated is a South Lake Union/ for curing them with gene therapy. step toward developing a complete picture of Ophthalmology, University Taking an empirical approach to of Washington, Box the diversity of ganglion cell types and their differentiating theories of color vision was a 358058, 750 Republican functions. Such knowledge could be useful in theme of the work of Frederick William Edridge- Street, Building E Room developing therapeutic strategies for blinding 184, Seattle, WA 98109, Green (1863–1953) as he performed experiments eye disorders that rely on stimulating USA illuminating what it means to be color blind and Tel: +1 206 5438065; elements in the retina, where more than 50 Fax: +1 206 6859315. different neuron types are organized into tried to discover the best ways color vision fi E-mail: [email protected] circuits that transform signals from de ciencies should be tested. We were very photoreceptors into specialized detectors privileged to give the Edridge-Green lecture at Received: 16 September many of which are not directly involved in The Royal College of Ophthalmologists Annual 2016 Congress at Birmingham in May 2016. This Accepted: 6 October 2016 conscious vision. Published online: Eye (2017) 31, 286–300; doi:10.1038/eye.2016.257; article is based on the material presented at that 9 December 2016 published online 9 December 2016 occasion. Evolution of the circuitry for conscious color vision in primates J Neitz and M Neitz 287 The world is not colorful for lower animals even though ‘Vision for conscious perception’ vs ‘Vision for action’ some have color vision Finally, mantis shrimp likely don’t ‘see’ at all in the sense A theme of this article is that there have been a huge we mean when we refer to our own vision. Our conscious number of, often contradictory, ideas about color vision vision is based on the neural pathway that projects and that evidence is required to determine which are most through the lateral geniculate nucleus (LGN) of the likely true. As an example, consider the discovery that the thalamus. In humans, interruption of this pathway results mantis shrimp has 12 spectrally different receptors, which in the loss of all conscious vision. There can be no led to speculation about their ‘exquisite’ color perception. conscious color perception without brain structures to In their article entitled ‘The colourful world of the mantis mediate it. The primate LGN is homologous to the dorsal shrimp,’ Marshall and Oberwinkler1 speculate that ‘the LGN in lower vertebrates and this structure did not remarkable colour-vision…befits their habitat of evolve until after the appearance of amphibians,4 kaleidoscopically colourful tropical coral reefs’. However, hundreds of millions of years after the appearance of the fi evidence from recent experiments2 demonstrates that rst eyes. fi these ideas are not true. Wavelength (λ) discrimination Thus, even though lights with suf ciently large was remarkably poor in mantis shrimp showing values of differences in spectral distribution can drive behavioral Δλ, the separation between wavelengths required for responses in the mantis shrimp, and, thus, they can be ‘ ’ discrimination, ranging between 12 and 25 nm whereas said to exhibit color vision their world is not coloured. ‘ ’ humans, with three cone photoreceptor types, require Δλ The title of this article refers to conscious color vision to values of only 2 nm or less across much of the spectrum. emphasize evidence presented here that humans have fi This illustrates that visual capacities cannot be inferred completely separate circuitry originating at the rst ‘ from the physiological properties of the detectors and synapse in the retina dedicated to conscious color vision- ’ how misled we can be by our intuitions. Color vision for-perception and this circuitry evolved independently and much later than the color vision circuitry that evolved capacities cannot be determined from knowing the to directly mediate action.5 number of spectrally different receptors. For example, humans have at least six spectrally different light sensors in our eye, three types of cones, peaking at 419, 530, and The human brain builds up a representation of the 559 nm, rods at 500 nm, melanopsin ganglion cells world around us in our cortex with a 480 nm spectral peak, and the newly discovered When we look at a scene, a visual representation is built OPN5-expressing3 ganglion cells peaking at 380 nm. up in our cortex. The brains of early vertebrates are However, we do not have six-dimensional color vision. missing the brain structures that we use when we say ‘the Our different light sensors evolved at different times for world is colored.’ For example, when an animal like a different functions. Although the spectral peaks of the frog looks out at a static unmoving scene it is completely individual receptor types were undoubtedly shaped blind to the world around him. A human can peruse the by evolutionary pressure, the differences between visual representation of the world inside his or her brain melanopsin at 480 nm, rhodopsin at 500 nm, and M cone and plot a course of action. Without moving at all, a opsin at 530 nm did not evolve to provide color person can decide to walk to the other side of a room and discrimination. Similarly, different receptors in the mantis based on an internal visual representation, plan a route to shrimp eye presumably evolved to serve different navigate around obstacles. It may be difficult to imagine, — functions, even some we lack such as polarization but a frog has little or no ability to use vision to do this. In — detection and the differences in spectral sensitivity lower vertebrates, the guidance of goal-directed and evidently evolved as the result of other pressures, not to navigating behaviors is dominated by other sensory provide extra dimensions of color vision. modalities, particularly olfaction. They do have a Two photoreceptors with spectrally different representation of space; it is just not a visual one. They photopigments do collectively have information for color use information from external, non-visual, stimuli along vision; however, the organism must have the biological with internal vestibular and proprioceptive inputs to machinery to extract it. People tend to have a strong determine their position and heading in space. In contrast intuition that organisms must be making use of all the to olfaction, vision in lower vertebrates is primarily information available to them without consideration of concerned with operating in real-time, mediating reflexive the evolutionary demands on the system. The most movements to pursue prey, avoid obstacles, and important lesson is that the only way we can tell if an predators as they are encountered. To serve this function, organism is making use of the information carried by retinal ganglion cells of lower animals have evolved as a particular neuron is to test it experimentally. detectors that are narrowly tuned to respond to trigger Eye Evolution of the circuitry for conscious color vision in primates J Neitz and M Neitz 288 features that have evolved to elicit particular actions from the yellow tail of a conspecific.
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