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ABSTRACT: The giraffe (Giraffa camelopardalis) is a browser that uses its extensible tongue to selectively collect leaves during foraging. As the tallest extant terrestrial mammal, its elevated head height provides panoramic surveillance of the environment. These aspects of the giraffe's ecology and phenotype suggest that vision is of prime importance. Using Nissl-stained retinal wholemounts and stereological methods, we quantitatively assessed the retinal specializations in the ganglion cell layer of the giraffe. The mean total number of retinal ganglion cells was 1,393,779 and their topographic distribution revealed the presence of a horizontal visual streak and a temporal area. With a mean peak of 14,271 cells/mm(2) , upper limits of spatial resolving power in the temporal area ranged from 25 to 27 cycles/degree. We also observed a dorsotemporal extension (anakatabatic area) that tapers toward the nasal retina giving rise to a complete dorsal arch. Using neurofilament-200 immunohistochemistry, we also detected a dorsal arch formed by alpha ganglion cells with density peaks in the temporal (14-15 cells/mm(2) ) and dorsonasal (10 cells/mm(2) ) regions. As with other artiodactyls, the giraffe shares the presence of a horizontal streak and a temporal area which, respectively, improve resolution along the horizon and in the frontal visual field. The dorsal arch is related to the giraffe's head height and affords enhanced resolution in the inferior visual field. The alpha ganglion cell distribution pattern is unique to the giraffe and enhances acquisition of motion information for the control of tongue movement during foraging and the detection of predators. J. Comp. Neurol. 521:2042-2057, 2013. © 2012 Wiley Periodicals, Inc.
The Journal of Comparative Neurology 06/2013; 521(9):2042-57. · 3.81 Impact Factor
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ABSTRACT: Abstract Irradiation in the red/near-infrared spectrum (R/NIR, 630-1000 nm) has been used to treat a wide range of clinical conditions, including disorders of the central nervous system (CNS), with several clinical trials currently underway for stroke and macular degeneration. However, R/NIR irradiation therapy (R/NIR-IT) has not been widely adopted in clinical practice for CNS injury or disease for a number of reasons, which include the following. The mechanism/s of action and implications of penetration have not been thoroughly addressed. The large range of treatment intensities, wavelengths and devices that have been assessed make comparisons difficult, and a consensus paradigm for treatment has not yet emerged. Furthermore, the lack of consistent positive outcomes in randomised controlled trials, perhaps due to sub-optimal treatment regimens, has contributed to scepticism. This review provides a balanced précis of outcomes described in the literature regarding treatment modalities and efficacy of R/NIR-IT for injury and disease in the CNS. We have addressed the important issues of specification of treatment parameters, penetration of R/NIR irradiation to CNS tissues and mechanism/s, and provided the necessary detail to demonstrate the potential of R/NIR-IT for the treatment of retinal degeneration, damage to white matter tracts of the CNS, stroke and Parkinson's disease.
Reviews in the neurosciences 03/2013; · 2.41 Impact Factor
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ABSTRACT: We report the discovery of light organs (photophores) adjacent to the dorsal defensive spines of a small deep-sea lanternshark (Etmopterus spinax). Using a visual modeling based on in vivo luminescence recordings we show that this unusual light display would be detectable by the shark's potential predators from several meters away. We also demonstrate that the luminescence from the spine-associated photophores (SAPs) can be seen through the mineralized spines, which are partially translucent. These results suggest that the SAPs function, either by mimicking the spines' shape or by shining through them, as a unique visual deterrent for predators. This conspicuous dorsal warning display is a surprising complement to the ventral luminous camouflage (counterillumination) of the shark.
Scientific Reports 02/2013; 3:1308.
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ABSTRACT: Sharks use highly sensitive electroreceptors to detect the electric fields emitted by potential prey. However, it is not known whether prey animals are able to modulate their own bioelectrical signals to reduce predation risk. Here, we show that some shark (Chiloscyllium punctatum) embryos can detect predator-mimicking electric fields and respond by ceasing their respiratory gill movements. Despite being confined to the small space within the egg case, where they are vulnerable to predators, embryonic sharks are able to recognise dangerous stimuli and react with an innate avoidance response. Knowledge of such behaviours, may inform the development of effective shark repellents.
PLoS ONE 01/2013; 8(1):e52551. · 4.09 Impact Factor
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ABSTRACT: Much is known regarding the evolution of colour vision in nearly every vertebrate class, with the notable exception of the elasmobranchs. While multiple spectrally distinct cone types are found in some rays, sharks appear to possess only a single class of cone and, therefore, may be colour blind. In this study, the visual opsin genes of two wobbegong species, Orectolobus maculatus and Orectolobus ornatus, were isolated to verify the molecular basis of their monochromacy. In both species, only two opsin genes are present, RH1 (rod) and LWS (cone), which provide further evidence to support the concept that sharks possess only a single cone type. Examination of the coding sequences revealed substitutions that account for interspecific variation in the photopigment absorbance spectra, which may reflect the difference in visual ecology between these species.
Biology letters 09/2012; · 3.76 Impact Factor
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ABSTRACT: 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.
Microscopy Research and Technique 05/2012; 75(9):1218-28. · 1.79 Impact Factor
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ABSTRACT: The electrosensory capabilities of wobbegong sharks are of particular interest, partly because very little is known about
their behavioural ecology and specifically because of their unusual ambush predatory strategy and benthic lifestyle. While
several biological functions of electroreception have been proposed, less consideration has been given to the functional significance
of interspecific differences in the morphology and topographic distribution of the ampullary organs. The morphology of the
ampullary organs was examined in four species of wobbegong shark, and the distribution of electroreceptive pores was mapped
in two species. The ampullary systems of wobbegongs are similar in morphology to other marine elasmobranchs. The number of
alveoli per ampullae is not significantly different between the four species; however, differences are seen between ampullary
cell size in some species. Ampullary pore distribution patterns are relatively unique, with the majority of pores occurring
on the dorsal region of the head. Wobbegongs feed primarily on demersal teleost fishes, and as the benthic and well-camouflaged
wobbegong remains motionless, these fish could be easily detected by the dorsal pores when swimming within range.
Marine Biology 04/2012; 158(4):723-735. · 2.28 Impact Factor
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ABSTRACT: Jawed fishes that possess an elongated rostrum use it to either sense prey or to manipulate it, but not for both. The billfish rostrum, for instance, lacks any sensory function and is used to stun prey [1], while paddlefishes use their rostrum to detect and orient towards electric fields of plankton [2]. Sturgeons search through the substrate with their electroreceptive rostrum, and engulf prey by oral suction [2]. Here, we show that juvenile freshwater sawfish Pristis microdon are active predators that use their toothed rostrum - the saw - to both sense prey-simulating electric fields and capture prey. Prey encountered in the water column is attacked with lateral swipes of the saw that can stun and/or impale it. We compare sawfish to shovelnose rays, which share a common shovelnose ray-like ancestor [3] and lack a saw.
Current biology: CB 03/2012; 22(5):R150-1. · 10.99 Impact Factor
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ABSTRACT: In the aquatic environment, living organisms emit weak dipole electric fields, which spread in the surrounding water. Elasmobranchs detect these dipole electric fields with their highly sensitive electroreceptors, the ampullae of Lorenzini. Freshwater sawfish, Pristis microdon, and two species of shovelnose rays, Glaucostegus typus and Aptychotrema rostrata were tested for their reactions towards weak artificial electric dipole fields. The comparison of sawfishes and shovelnose rays sheds light on the evolution and function of the elongated rostrum ('saw') of sawfish, as both groups evolved from a shovelnose ray-like ancestor. Electric stimuli were presented both on the substrate (to mimic benthic prey) and suspended in the water column (to mimic free-swimming prey). Analysis of around 480 behavioural sequences shows that all three species are highly sensitive towards weak electric dipole fields, and initiate behavioural responses at median field strengths between 5.15 and 79.6 nV cm(-1). The response behaviours used by sawfish and shovelnose rays depended on the location of the dipoles. The elongation of the sawfish's rostrum clearly expanded their electroreceptive search area into the water column and enables them to target free-swimming prey.
PLoS ONE 01/2012; 7(7):e41605. · 4.09 Impact Factor
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ABSTRACT: Little is known about the sensory abilities of elasmobranchs (sharks, skates and rays) compared with other fishes. Despite their role as apex predators in most marine and some freshwater habitats, interspecific variations in visual function are especially poorly studied. Of particular interest is whether they possess colour vision and, if so, the role(s) that colour may play in elasmobranch visual ecology. The recent discovery of three spectrally distinct cone types in three different species of ray suggests that at least some elasmobranchs have the potential for functional trichromatic colour vision. However, in order to confirm that these species possess colour vision, behavioural experiments are required. Here, we present evidence for the presence of colour vision in the giant shovelnose ray (Glaucostegus typus) through the use of a series of behavioural experiments based on visual discrimination tasks. Our results show that these rays are capable of discriminating coloured reward stimuli from other coloured (unrewarded) distracter stimuli of variable brightness with a success rate significantly different from chance. This study represents the first behavioural evidence for colour vision in any elasmobranch, using a paradigm that incorporates extensive controls for relative stimulus brightness. The ability to discriminate colours may have a strong selective advantage for animals living in an aquatic ecosystem, such as rays, as a means of filtering out surface-wave-induced flicker.
Journal of Experimental Biology 12/2011; 214(Pt 24):4186-92. · 3.00 Impact Factor
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ABSTRACT: 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.
Journal of Morphology 11/2011; 273(4):423-40. · 1.54 Impact Factor
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ABSTRACT: Sea snakes have evolved numerous anatomical, physiological, and behavioral adaptations to suit their wholly aquatic lifestyle. However, although sea snakes use vision for foraging and mate selection, little is known about their visual abilities. We used microspectrophotometry, light microscopy, and scanning electron microscopy to characterize the retinal photoreceptors of spine-bellied (Lapemis curtus) and horned (Acalyptophis peronii) sea snakes. Both species have three types of visual pigment sensitive to short (SWS; wavelength of maximum absorbance, λmax 428-430 nm), medium (MWS; λmax 496 nm), and long wavelengths of light (LWS; λmax 555-559 nm) in each of three different subtypes of cone-like single photoreceptor. They also possess a cone-like double photoreceptor subtype, both the principal and accessory member of which contain the LWS visual pigment. Conventional rods were not observed, although the MWS photoreceptor may be a "transmuted" rod. We also used stereology to measure the total number and topographic distribution of neurons in the ganglion cell layer of L. curtus, the olive sea snake (Aipysurus laevis), and the olive-headed sea snake (Disteira major). All species have a horizontal visual streak with specialized areas in the nasal and temporal retina. Both L. curtus and D. major also have a specialized area in the ventral retina, which may reflect differences in habitat usage and/or foraging behavior compared to A. laevis. Maximal spatial resolution was estimated at 1.1, 1.6, and 2.3 cycles deg⁻¹ in D. major, L. curtus, and A. laevis, respectively; the superior value for A. laevis may reflect its specialized crevice-foraging hunting technique.
The Journal of Comparative Neurology 10/2011; 520(6):1246-61. · 3.81 Impact Factor
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ABSTRACT: Traumatic injury to the central nervous system (CNS) is accompanied by the spreading damage of secondary degeneration, resulting in further loss of neurons and function. Partial transection of the optic nerve (ON) has been used as a model of secondary degeneration, in which axons of retinal ganglion cells in the ventral ON are spared from initial dorsal injury, but are vulnerable to secondary degeneration. We have recently demonstrated that early after partial ON injury, oxidative stress spreads through the ventral ON vulnerable to secondary degeneration via astrocytes, and persists in the nerve in aggregates of cellular debris. In this study, we show that diffuse transcranial irradiation of the injury site with far red to near infrared (NIR) light (WARP 10 LED array, center wavelength 670 nm, irradiance 252 W/m(-2), 30 min exposure), as opposed to perception of light at this wavelength, reduced oxidative stress in areas of the ON vulnerable to secondary degeneration following partial injury. The WARP 10 NIR light treatment also prevented increases in NG-2-immunopositive oligodendrocyte precursor cells (OPCs) that occurred in ventral ON as a result of partial ON transection. Importantly, normal visual function was restored by NIR light treatment with the WARP 10 LED array, as assessed using optokinetic nystagmus and the Y-maze pattern discrimination task. To our knowledge, this is the first demonstration that 670-nm NIR light can reduce oxidative stress and improve function in the CNS following traumatic injury in vivo.
Journal of neurotrauma 11/2010; 27(11):2107-19. · 4.25 Impact Factor
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ABSTRACT: Several visual traits have previously been assessed in elasmobranchs; however, few studies have examined and compared multiple visual attributes within a particular genus. The primary advantage of studying closely related species is that any differences between them are more likely to reflect functional ecological adaptations rather than the effects of phylogenetic separation. In this study, the visual capabilities of 4 wobbegong shark species, which vary in life-history and/or habitat, were examined: the western wobbegong (Orectolobus hutchinsi), the spotted wobbegong (O. maculatus), the ornate wobbegong (O. ornatus) and the dwarf spotted wobbegong (O. parvimaculatus). The retinae of all 4 wobbegong species are duplex; rod and cone photoreceptors can be distinguished easily on the basis of morphology. Some variation in relative eye size exists, with O. parvimaculatus possessing the largest eyes. The topographic distribution of cells within the ganglion cell layer of O. hutchinsi reveals a weakly elongated central visual streak of increased cell density, mediating a higher spatial resolving power of 2.06 cycles deg⁻¹ in the frontal visual field. Retinal topography of O. maculatus and O. parvimaculatus is similar, with both possessing a dorsal horizontal streak facilitating an increased spatial resolving power of 3.51 cycles deg⁻¹ and 3.91 cycles deg⁻¹, respectively, in the lower visual field. O. parvimaculatus also possesses an area of increased cell density in the naso-ventral region of the retina, mediating acute vision in the upper caudal region of the visual field. While all 4 species have visual systems optimised for increased visual sensitivity, O. maculatus and O. parvimaculatus appear to be particularly well suited to activity under low light conditions.
Brain Behavior and Evolution 11/2010; 76(3-4):248-60. · 2.21 Impact Factor
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ABSTRACT: Archerfish are famous for spitting jets of water to capture terrestrial insects, a task that not only requires oral dexterity, but also the ability to detect small camouflaged prey against a visually complex background of overhanging foliage. Because detection of olfactory, auditory and tactile cues is diminished at air-water interfaces, archerfish must depend almost entirely on visual cues to mediate their sensory interactions with the aerial world. During spitting, their eyes remain below the water's surface and must adapt to the optical demands of both aquatic and aerial fields of view. These challenges suggest that archerfish eyes may be specially adapted to life at the interface between air and water. Using microspectrophotometry to characterize the spectral absorbance of photoreceptors, we find that archerfish have differentially tuned their rods and cones across their retina, correlated with spectral differences in aquatic and aerial fields of view. Spatial resolving power also differs for aquatic and aerial fields of view with maximum visual resolution (6.9 cycles per degree) aligned with their preferred spitting angle. These measurements provide insight into the functional significance of intraretinal variability in archerfish and infer intraretinal variability may be expected among surface fishes or vertebrates where different fields of view vary markedly.
Proceedings of the Royal Society B: Biological Sciences 04/2010; 277(1694):2607-15. · 5.41 Impact Factor
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ABSTRACT: Box jellyfish (Cubomedusae) possess a unique visual system comprising 24 eyes of four morphological types. Moreover, box jellyfish display several visually guided behaviours, including obstacle avoidance and light-shaft attractance. It is largely unknown what kind of visual information box jellyfish use for carrying out these behaviours. Brightness contrast is almost certainly involved, but it is also possible that box jellyfish extract colour information from their surroundings. The possible presence of colour vision in box jellyfish has previously been investigated using behavioural, electrophysiological and immunohistochemical methods. However, the results from these studies are to some degree conflicting and inconclusive. Here, we present results from an investigation into the visual system of the box jellyfish Chiropsella bronzie, using microspectrophotometry and immunohistochemistry. Our results strongly indicate that only one type of visual pigment is present in the upper and lower lens eyes with a peak absorbance of approximately 510 nm. Additionally, the visual pigment appears to undergo bleaching, similar to that of vertebrate visual pigments.
Proceedings of the Royal Society B: Biological Sciences 02/2010; 277(1689):1843-8. · 5.41 Impact Factor
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ABSTRACT: Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinal bauplan to be used by all subsequent vertebrate descendents. Image-forming eyes were under tremendous selection pressure and the ability to identify suitable prey and detect potential predators was thought to be one of the major drivers of speciation in the Early Cambrian. Based on the fossil record, we know that hagfishes, lampreys, holocephalans, elasmobranchs and lungfishes occupy critical stages in vertebrate evolution, having remained relatively unchanged over hundreds of millions of years. Now using extant representatives of these 'living fossils', we are able to piece together the evolution of vertebrate photoreception. While photoreception in hagfishes appears to be based on light detection and controlling circadian rhythms, rather than image formation, the photoreceptors of lampreys fall into five distinct classes and represent a critical stage in the dichotomy of rods and cones. At least four types of retinal cones sample the visual environment in lampreys mediating photopic (and potentially colour) vision, a sampling strategy retained by lungfishes, some modern teleosts, reptiles and birds. Trichromacy is retained in cartilaginous fishes (at least in batoids and holocephalans), where it is predicted that true scotopic (dim light) vision evolved in the common ancestor of all living gnathostomes. The capacity to discriminate colour and balance the tradeoff between resolution and sensitivity in the early vertebrates was an important driver of eye evolution, where many of the ocular features evolved were retained as vertebrates progressed on to land.
Philosophical Transactions of The Royal Society B Biological Sciences 11/2009; 364(1531):2925-40. · 6.40 Impact Factor
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ABSTRACT: Animals change their body coloration for a variety of purposes including communication, thermoregulation and crypsis. The cues that trigger adaptive colour change are often unclear, and the role of colour vision remains largely untested. Here, we investigated the bluestriped fangblenny (Plagiotremus rhinorhynchos), an aggressive mimic that changes its body coloration to impersonate a variety of coral reef fishes. In this field, we determined the fish species that the fangblenny associated with and measured the spectral reflectance of mimics and their models. We measured the spectral absorbance characteristics of the retinal photoreceptor visual pigments in the bluestriped fangblenny using microspectrophotometry and found it to have rod photoreceptors (lambda(max) 498 nm), single cones (449 nm) and double cones (561 nm principal member; 520 nm accessory member). Using theoretical vision models, fangblennies could discriminate between the colours they adopted and the colours of the fish they associated with. Potential signal receivers (Abudefduf abdominalis and Ctenochaetus strigosus) perceived colours of most mimics to closely resemble fishes they associated with. However, fishes with ultraviolet-sensitive visual pigments were better at discriminating between mimics and models. Therefore, colour vision could be used by fangblennies when initiating colour change enabling them to accurately resemble fishes they associate with and to avoid detection by signal receivers.
Proceedings of the Royal Society B: Biological Sciences 06/2009; 276(1662):1565-73. · 5.41 Impact Factor
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ABSTRACT: Elasmobranchs are thought to possess an acute sense of smell, but the relationship between the anatomy of their olfactory organs and their sensory ecology is poorly understood. Moreover, the ecological diversity of elasmobranchs as a group indicates that there might be considerable interspecific variation in the importance of the olfactory sense. Wobbegong sharks, with their sedentary lifestyle and ambush predatory technique, probably utilize their senses differently than other shark species, making it difficult to generalize about their olfactory capabilities and olfaction-dependent behaviors. In this study, the number of olfactory lamellae and the surface area of the olfactory epithelium were measured as a means of assessing relative olfactory sensitivity in four species of wobbegong shark (the Western wobbegong, Orectolobus hutchinsi; the spotted wobbegong, O. maculatus; the ornate wobbegong, O. ornatus; and the dwarf spotted wobbegong, O. parvimaculatus). We also present a phylogenetic comparative analysis between wobbegongs and other elasmobranchs for which published data on olfactory morphology are available. There is a significant difference in the total number of olfactory lamellae between most species, but not between O. hutchinsi and O. maculatus, although the olfactory sensory surface area is comparable between these two species and O. ornatus. Orectolobus parvimaculatus has a significantly larger olfactory sensory surface area than the other three species, and there is a positive relationship between total body length and olfactory sensory surface area for all four species. Assuming that these morphological measures are true indications of olfactory capability, the olfactory abilities of wobbegongs are as good as, or better than, other benthic elasmobranchs. Interspecific differences in olfactory ability within this group of benthic ambush predators could indicate relative differences in prey detection, intraspecific recognition and mate detection.
Brain Behavior and Evolution 04/2009; 73(2):91-101. · 2.21 Impact Factor
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ABSTRACT: The development of the eye of the oviparous brown banded bamboo shark, Chiloscyllium punctatum, was monitored from egg deposition through adulthood. The order and timing of retinal cell differentiation were assessed by light and transmission electron microscopy. As in other vertebrates, the ganglion cells are the first to differentiate, in this case by 81 days post-egg deposition (dpd). The order then deviates from what is typically quoted for vertebrates, with the Müller and amacrine cells differentiating morphologically around the same time, followed by the bipolar cells (101 dpd) and finally the horizontal cells and photoreceptors (124 dpd). The neural retina is fully differentiated and synaptic connections are formed approximately 1 month prior to hatching, which occurs at about 158 dpd. The mature retina is duplex, with a peak rod to cone ratio of approximately 12:1. The eye and lens of C. punctatum continue to grow throughout life and become less aspherical with growth; the equatorial (nasotemporal) lens diameter is 12% larger than the axial (anterior-posterior) lens diameter in embryos and 8% larger in adults. Access to developmental stages and the protracted gestational period of C. punctatum make it a highly valuable model for developmental studies of the visual system. This study also provides an evolutionary perspective on retinal neurogenesis in an elasmobranch.
The Journal of Comparative Neurology 01/2009; 513(1):83-97. · 3.81 Impact Factor
