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PROCESSES in BIOLOGICAL VISION: Including PROCESSES IN BIOLOGICAL VISION: including, ELECTROCHEMISTRY OF THE NEURON This material is excerpted from the full β-version of the text. The final printed version will be more concise due to further editing and economical constraints. A Table of Contents and an index are located at the end of this paper. James T. Fulton Vision Concepts [email protected] April 30, 2017 Copyright 2004 James T. Fulton The Retina 3- 1 3 Description of the Retina1 3.1 Introduction A major finding of this work is that the retinula of the Insecta and some Mollusca eyes do not employ opsin as a substrate for the appropriate chromophores, which remain the rhodopsin()’s of the retinine family (section 3.6). The retinines are deposited directly on the villi emanating from the dendrites of the sensory receptor neurons. This finding has wide ramifications relating to the conventional concepts of the sensory receptors of Chordata. The opsin of these sensory receptors is used to control the orientation of the retinine liquid crystalline chromophores. It does not participate in the transduction process. Innumerable representations of the retina appear in the literature, at all different scales and using every imaginable artistic technique. Most of them do not show an absolute scale or even the coordinates of the retinal area being discussed. They virtually never show the direction and optical quality of the incident radiation or the location of the focal plane of the optical system. When these parameters are used as a foundation of discussion, many sketches, photographs and electron micrographs are found inadequate. Some become interpretable from a different perspective. The purpose of this Chapter is to provide a more comprehensive view of the retina, including a more coordinated description of the different zones of the retina, and a broader understanding of the top level architecture of the visual signaling system pertaining to the retina. Recently, good progress has been made in determining the distribution of different chromophorically sensitive photoreceptors in the retina. However, the results are still largely statistical. Initially, this chapter will examine all photosensitive surfaces that contribute to the visual capabilities of an animal. In this context, the group of retinula found in the eyes of Arthropoda will be considered a retina. This provides a useful element in the development of an overall framework for discussing the retina. Traditionally, the eyes of animals have been separated into two categories, vertebrate and invertebrate. Complete books have been written based on this distinction2. Bernhard has provided a comprehensive study of the compound eye3. Laughlin has provided an extensive comparison between these two categories4. However, this use of a dichotomy is constraining. As discussed briefly in Chapter 1, there are clearly three categories of eyes that are well aligned with the conventional phylogenic tree. These are the compound eye, and its prototypical simple eye, of Arthropoda, the complex eye with a direct retina of Mollusca, and the complex eye with a reversed retina of Chordata. Evolution has led to incongruities within this classification but they are minor–and illustrative. This work will employ the above trichotomy instead of the conventional dichotomy. The above trichotomy provides a much better framework for interpreting both the detailed form of the types of photoreceptor cells found in eyes and the degree of structure in the retinas of these phyla. The above trichotomy of eye types should not be confused with the spectral capability of eyes. The fundamental architecture of biological vision is tetrachromatic. Provision is made in the photochemistry of vision to form photoreceptors of four spectral types and many superfamilies and families of animals are tetrachromatic. It is only within phyla that one finds trichromats and they are of two distinct types. Arthropoda are generally short wavelength trichromats, employing photoreceptors sensitive to the ultraviolet, short and medium wavelength spectral ranges. Chordata are generally tetrachromatic, except in the physically larger animals and sometimes as a result of evolution to satisfy an ecological niche. Tetrachromats have photoreceptors sensitive to the ultraviolet, short, medium and long wavelength regions of the visible spectrum. Many birds5, fish and rodents are known to be tetrachromatic. Tetrachromaticity is common among fish6. However, many species exhibit tetrachromatic vision as 1Released: April 30, 2017 2Autrum, H. ed. (1979) Comparative Physiology and Evolution of Vision in Invertebrates: A. Invertebrate Photoreceptors. NY: Springer-Verlag 3Bernhard, C. (1965) The Functional Organization of the Compound Eye. NY: Pergamon Press 4Laughlin, S. (1981) Common principles for vertebrate and invertebrate visual systems. In Handbook of Sensory Physiology, Vol. VII/6B, “Comparative physiology and evolution of vision in invertebrates,” Autrum, H. ed. NY: Springer-Verlag pg. 263 5Altshuler, D. et. al. Xxx Evol. Ecol. Res. vol. 3, p 767 6Neumeyer, C. & Arnold, K. (1989) Tetrachromatic colour vision in goldfish and turtle. Xxx In 2 Processes in Biological Vision juveniles but frequently change to long wavelength trichromats with age (or more fundamentally, as the lens group grows and thickens). The larger members of Chordata, particularly the larger terrestrial members such as Human, have lost their ultraviolet sensitivity due to the thickness of the lens group serving the eye. It is not clear that the retinas of all large Chordata have completely lost their ultraviolet capability through evolution. Humans exhibit at least some ultraviolet capability when the lens group is removed. The large chordates are long wavelength trichromats, having photoreceptors sensitive to the short, medium and long wavelength portions of the visual spectrum. The data available for Mollusca is inadequate to determine their general capability. 3.1.1 Background 3.1.1.1 Order and tetra-chromaticity in the photoreceptor arrays of the retinas By examining the trichotomy of animal retinas, there is a clear trend with regard to the statistical order of the arrays of photoreceptors. There also appears to be an order with respect to these arrays in many animals as a function of their maturity. Franceschini has provided a striking example of the orderliness of the retinal array in Arthropoda7. This orderliness even extends to the lamina behind the retina. The orderliness is clearly traceable to the prototypical simple eye. The orderliness is reminiscent of that of a crystalline structure. Bowmaker & Kunz have described a similar level of orderliness in the immature brown trout8. They noted that the orderliness appeared to fall with age and surmised that the ultraviolet photoreceptors tended to disappear from the retina. Their images were primarily of small areas of the retina. Their spectrograms of the four chromophores of vision, although somewhat limited at the extreme wavelengths and plotted on a normalized linear ordinate, are in close agreement with those predicted by this work. Kouyama & Marshak studied the statistics of two mosaics of retinal neurons in the primate retina9. The areas were in the mid-periphery, typically six millimeters from the macaque fovea, and consisted of about 150 photoreceptors and about twice as many signal processing neurons described as bipolar cells. Unfortunately, they did not employ optical stimuli to excite the arrays. They employed staining of what were believed to be photoreceptors and bipolar cells associated with the short wavelength spectral channels of vision. Therefore, the arrays were not directly correlated with the spectral performance of the visual system. Chan, et. al. provide both morphology and statistics on the distribution of horizontal cells of the 1st lateral matrix in new world monkeys, with some comparisons with the macaque monkey10. They provide a picture of one horizontal cell, at 6.9 millimeters from the fovea, with a neuritic arborization of less than 50 microns in diameter but an axon that is 958 microns long. This length approaches the maximum reported for neurons processing signals in the electrotonic (analog) domain. Chan, et. al. also reference the paper by Dacey defining two distinct types of horizontal cells that appear to correspond to the P-channel and Q-channel horizontal cells of this work11. The H2 horizontal cells respond to short wavelength stimulation. Both the H1 and H2 type cells respond to mid-wavelength stimulation. The H1 type cells respond to both mid and long wavelength stimulation but do not respond to short wavelength stimulation. The H1 cells generate Q-channel chrominance signals and the H2 cells generate P-channel chrominance signals according to the nomenclature of this work. Chan, et. al. confirm the polymorphism of color vision in the marmoset based primarily on their ability to get it to make color matches following training. They claim trichromatism in females of that family. However, they claim the other animals are dichromats because they did not respond. 7Franceschini, N. (1985) XXX 8Bowmaker, J. & Kunz, Y. (1987) Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the broun trout (Salmo trutta): age-dependent changes. Vision Res. vol. 27, no. 12, pp. 2101-2108 9Kouyama, N. & Marshak, D. (1997) The topographical relationship between two neuronal mosaics in the short wavelength-sensitive system of the primate retina. Visual Neuroscience, vol. 14, pp. 159-167 10Chan,
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