Functional significance of the taper of vertebrate cone photoreceptors

© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Journal of General Physiology 139 (2012): 159-187, doi:10.1085/jgp.201110692.Vertebrate photoreceptors are commonly distinguished based on the shape of their outer segments: those of cones taper, whereas the ones from rods do not. The functional advantages of cone taper, a common occurrence in vertebrate retinas, remain elusive. In this study, we investigate this topic using theoretical analyses aimed at revealing structure–function relationships in photoreceptors. Geometrical optics combined with spectrophotometric and morphological data are used to support the analyses and to test predictions. Three functions are considered for correlations between taper and functionality. The first function proposes that outer segment taper serves to compensate for self-screening of the visual pigment contained within. The second function links outer segment taper to compensation for a signal-to-noise ratio decline along the longitudinal dimension. Both functions are supported by the data: real cones taper more than required for these compensatory roles. The third function relates outer segment taper to the optical properties of the inner compartment whereby the primary determinant is the inner segment’s ability to concentrate light via its ellipsoid. In support of this idea, the rod/cone ratios of primarily diurnal animals are predicted based on a principle of equal light flux gathering between photoreceptors. In addition, ellipsoid concentration factor, a measure of ellipsoid ability to concentrate light onto the outer segment, correlates positively with outer segment taper expressed as a ratio of characteristic lengths, where critical taper is the yardstick. Depending on a light-funneling property and the presence of focusing organelles such as oil droplets, cone outer segments can be reduced in size to various degrees. We conclude that outer segment taper is but one component of a miniaturization process that reduces metabolic costs while improving signal detection. Compromise solutions in the various retinas and retinal regions occur between ellipsoid size and acuity, on the one hand, and faster response time and reduced light sensitivity, on the other.This work was funded by the Natural Sciences and Engineering Research Council of Canada Discovery Grant 238886 and a Grass-Marine Biological Laboratory Sabbatical Fellowship in Neurosciences to I. Novales Flamarique.2012-07-1

The physiological tolerance of the grey carpet shark (Chiloscyllium punctatum) and the epaulette shark (Hemiscyllium ocellatum) to anoxic exposure at three seasonal temperatures

The epaulette shark (Hemiscyllium ocellatum) and the grey carpet shark (Chiloscyllium punctatum) are commonly found in periodically hypoxic environments. The ecophysiological time available for these animals to safely exploit these niches during different seasonal temperatures was examined. The time to loss of righting reflex (T (LRR)) was examined in response to an open ended anoxic challenge at three seasonal temperatures (23, 25 and 27A degrees C). Ventilation rates were measured in an open ended anoxic challenge at 23A degrees C and during 1.5 h of anoxia followed by 2 h of re-oxygenation at 23 and 25A degrees C. The mean T (LRR) of epaulette and grey carpet sharks was inversely proportional to temperature. The T (LRR) was similar between species at 23A degrees C; however, grey carpet sharks had significantly reduced T (LRR) at higher temperatures. During the standardised anoxic challenge, epaulette sharks entered into ventilatory depression significantly earlier at 25A degrees C. During re-oxygenation, epaulette sharks exposed to anoxia at 23A degrees C had no significant increase in ventilation rates. However, after anoxic challenge and re-oxygenation at 25A degrees C, epaulette sharks showed a significant increase in ventilation rates during re-oxygenation. Grey carpet sharks displayed no evidence of ventilatory depression during anoxia. However, during re-oxygenation, grey carpet sharks had significantly elevated ventilation rates above pre-experimental levels and control animals. These data demonstrate that the anoxia tolerance times of both species were temperature dependent, with a significant reduction in the T (LRR) occurring at higher temperatures. Epaulette sharks had a significantly greater T (LRR) at higher temperatures than grey carpet sharks, which did not enter into a ventilatory depression

Ontogenetic changes in retinal ganglion cell distribution and spatial resolving power in the brown-banded bamboo shark Chiloscyllium punctatum (Elasmobranchii)

The development of the visual system in anamniotic vertebrates is a continual process, allowing for ontogenetic changes in retinal topography and spatial resolving power. We examined the number and distribution of retinal ganglion cells in wholemounted retinae throughout the protracted embryonic development (∼5 months) of a chondrichthyan, i.e. the brown-banded bamboo shark Chiloscyllium punctatum, from the beginning of retinal cell differentiation (approximately halfway through embryogenesis) to adulthood. We also identified and quantified the number of apoptosed cells within the ganglion cell layer to evaluate the contribution of apoptosis to changes in retinal topography. C. punctatum undergoes rapid changes in ganglion cell distribution during embryogenesis, where high levels of apoptosis, especially around the retinal periphery, result in relative increases in ganglion cell density in the central retina which progressively extend nasally and temporally to form a meridional band at hatching. After hatching, C. punctatum forms and maintains a horizontal streak, showing only minor changes in topography during growth, with basal levels of apoptosis. The total number of retinal ganglion cells reaches 547,881 in adult sharks, but the mean (3,228 cells·mm⁻²) and peak (4,983 cells·mm⁻²) retinal ganglion cell densities are highest around the time of hatching. Calculated estimates of spatial resolving power, based on ganglion cell spacing (assuming a hexagonal mosaic) and assessment of the focal length from cryosections of the eye, increase from 1.47 cycles·degree ⁻¹ during embryogenesis to 4.29 cycles·degree⁻¹ in adults. The increase in spatial resolving power across the retinal meridian would allow this species to hunt and track faster, more mobile prey as it reaches maturity.15 page(s

Optimal preservation of the shark retina for ultrastructural analysis: an assessment of chemical, microwave, and high-pressure freezing fixation techniques

Recent advances in microwave chemical fixation (MCF) and/or high pressure freezing (HPF) combined with transmission electron microscopy have resulted in superior ultrastructural detail in a variety of tissue types. To date, selachian tissue has been fixed and processed using only standard chemical fixation (CF) methods, and the resulting ultrastructure has been less than ideal. In this study, we compared the ultrastructure of the fragile retinal tissue from the brown banded bamboo shark, Chiloscyllium punctatum, obtained using CF, MCF, and HPF methods. For all fixation protocols, ultrastructural preservation was improved by keeping the tissue in oxygenated Ringer solution until the time of fixation. Both MCF and HPF produced superior retinal ultrastructure compared to conventional CF. Although HPF occasionally resulted in very high quality ultrastructure, microwave fixation was almost comparable, quicker and far more consistent

Comparative retinal anatomy in four species of elasmobranch

Using both light and transmission electron microscopy, we examined the retinal anatomy of four elasmobranch species with differing ecologies: the bull shark Carcharhinus leucas, Port Jackson shark Heterodontus portusjacksoni, epaulette shark Hemiscyllium ocellatum and pink whipray Himantura fai. Their retinas are typical of other vertebrates, having three nuclear and two synaptic layers, but are characterised by very large horizontal cells, low densities of ganglion cells (many of which are displaced to the inner nuclear and inner plexiform layers) and the presence of numerous myelinated axons within the nerve fibre layer. Carcharhinus leucas, H. fai and H. ocellatum have duplex retinas containing both rods and single cones. The peak ratio of rods to cones is much lower in C. leucas (4:1) and H. fai (3:1) compared to H. ocellatum (19:1), reflecting differences in diel activity patterns. No cones were observed in the retina of H. portusjacksoni, which is strongly nocturnal. The cones of H. fai lack a distinct myoid and their nuclei are located in a discrete layer sclerad to the external limiting membrane (ELM), whereas those of C. leucas and H. ocellatum have an obvious myoid, and their nuclei are located vitread to the ELM. No double/twin cones were observed in any species. Incorporating data from other studies, there is a clear correlation between rod outer segment volume and visual ecology in elasmobranchs, with smaller volumes found in partly diurnal pelagic species and larger volumes in benthic nocturnal species. This trend may reflect fundamental differences in visual temporal resolution between active and more sedentary species

Vision in elasmobranchs and their relatives: 21st century advances

This review identifies a number of exciting new developments in the understanding of vision in cartilaginous fishes that have been made since the turn of the century. These include the results of studies on various aspects of the visual system including eye size, visual fields, eye design and the optical system, retinal topography and spatial resolving power, visual pigments, spectral sensitivity and the potential for colour vision. A number of these studies have covered a broad range of species, thereby providing valuable information on how the visual systems of these fishes are adapted to different environmental conditions. For example, oceanic and deep-sea sharks have the largest eyes amongst elasmobranchs and presumably rely more heavily on vision than coastal and benthic species, while interspecific variation in the ratio of rod and cone photoreceptors, the topographic distribution of the photoreceptors and retinal ganglion cells in the retina and the spatial resolving power of the eye all appear to be closely related to differences in habitat and lifestyle. Multiple, spectrally distinct cone photoreceptor visual pigments have been found in some batoid species, raising the possibility that at least some elasmobranchs are capable of seeing colour, and there is some evidence that multiple cone visual pigments may also be present in holocephalans. In contrast, sharks appear to have only one cone visual pigment. There is evidence that ontogenetic changes in the visual system, such as changes in the spectral transmission properties of the lens, lens shape, focal ratio, visual pigments and spatial resolving power, allow elasmobranchs to adapt to environmental changes imposed by habitat shifts and niche expansion. There are, however, many aspects of vision in these fishes that are not well understood, particularly in the holocephalans. Therefore, this review also serves to highlight and stimulate new research in areas that still require significant attention