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.     

Warm brain and eye temperatures in sharks

Temperatures in the brain and eyes of mako and porbeagle sharks (Lamnidae) are 5 degrees C warmer than the water while the brain and eye temperatures in six other species of pelagic sharks are within 0.1 degrees C of water temperature. An orbital rete mirabile is present in the porbeagle and mako sharks but absent in the cranial vasculature of eleven other species of pelagic sharks. The orbital rete in the head of the porbeagle and mako sharks acts as a heat exchanger which conserves metabolic heat and raises the local tissue temperatures. This brain and eye warming system should buffer the central nervous system from the effects of rapid temperature change. Warming of the retina may improve the visual sensitivity of these active predators.     

Photon Hunting in the Twilight Zone: Visual Features of Mesopelagic Bioluminescent Sharks

The mesopelagic zone is a visual scene continuum in which organisms have developed various strategies to optimize photon capture. Here, we used light microscopy, stereology-assisted retinal topographic mapping, spectrophotometry and microspectrophotometry to investigate the visual ecology of deep-sea bioluminescent sharks [four etmopterid species (Etmopterus lucifer, E. splendidus, E. spinax and Trigonognathus kabeyai) and one dalatiid species (Squaliolus aliae)]. We highlighted a novel structure, a translucent area present in the upper eye orbit of Etmopteridae, which might be part of a reference system for counterillumination adjustment or acts as a spectral filter for camouflage breaking, as well as several ocular specialisations such as aphakic gaps and semicircular tapeta previously unknown in elasmobranchs. All species showed pure rod hexagonal mosaics with a high topographic diversity. Retinal specialisations, formed by shallow cell density gradients, may aid in prey detection and reflect lifestyle differences; pelagic species display areae centrales while benthopelagic and benthic species display wide and narrow horizontal streaks, respectively. One species (E. lucifer) displays two areae within its horizontal streak that likely allows detection of conspecifics'' elongated bioluminescent flank markings. Ganglion cell topography reveals less variation with all species showing a temporal area for acute frontal binocular vision. This area is dorsally extended in T. kabeyai, allowing this species to adjust the strike of its peculiar jaws in the ventro-frontal visual field. Etmopterus lucifer showed an additional nasal area matching a high rod density area. Peak spectral sensitivities of the rod visual pigments (λ_max) fall within the range 484–491 nm, allowing these sharks to detect a high proportion of photons present in their habitat. Comparisons with previously published data reveal ocular differences between bioluminescent and non-bioluminescent deep-sea sharks. In particular, bioluminescent sharks possess higher rod densities, which might provide them with improved temporal resolution particularly useful for bioluminescent communication during social interactions.     

Variation in compound eye structure: effects of diet and family

Studies of compound eyes have revealed that variation in eye structure can substantially affect visual performance. Here, we investigate the degree to which a stressful rearing environment, which decreases body size, affects the eye phenotype. Full siblings of the Orange Sulphur butterfly, Colias eurytheme, were collected from known parents and split within families among two diet treatments that varied in quality. In both sexes, individuals reared on the high-quality diet had larger eye height and anterior facet diameter, and therefore, by inference, superior vision. However, relative to their reduced body size, individuals reared on low-quality diet had proportionally larger eyes and facets than individuals reared on high-quality diet. We interpret this finding as evidence that butterflies encountering nutritional stress increased proportional investment in eye development to reduce loss of visual performance. We also found significant broad-sense genetic variation underlying eye structure in both males and females, and report novel heritability estimates for eye height and facet diameter. Surprisingly, there was greater genetic variation in eye height among males than among females, despite apparently stronger directional selection on male vision. We discuss the implications of these data for our understanding of eye development and evolution.     

影响人眼视觉质量的光学因素

人眼作为一种光学器官,存在着一些光学缺陷,从物理学的角度分析了小瞳孔的衍射效应、眼球光学系统的像差、瞳孔尺寸、照明度和光学散射等对人眼视觉质量的影响。重点分析了由眼球的屈光介质引入的光学像差对人眼视觉质量的影响。     

夜行性昆虫微光视觉行为及其视觉适应机制

作为昆虫种群的重要组成部分,夜行性昆虫成功进化出了与其生存环境相适应的感觉机制,普遍认为夜行性昆虫主要依靠嗅觉和机械性感受等来探索环境,其视觉器官发生了退化或功能丧失。近年来,随着红外夜视、视网膜电位(electroretinogram, ERG)和视觉神经等生物新技术的应用,昆虫视觉生态学研究出现了突破性进展,自2002年以来陆续发现蛾类、蜜蜂和蜣螂等夜行性昆虫进化出了非凡的微光视觉(dim-light vision)能力,在夜晚(光照强度低于0.3 lx)依然可以如同在明亮的白天一样清晰、准确地感知目标物体特定的视觉特性,如明暗、颜色、形状、大小、对比度、偏振光和运动状态等,展现出视觉调控夜行性昆虫行为活动的巨大潜力。此外,这些夜行性昆虫复眼瞳孔、小眼焦距、视杆和色素颗粒等方面进化出了一些相应的形态生理特征,以提高光学灵敏度适应夜间微光环境。鉴于夜行性昆虫微光视觉行为及其视觉适应机制的研究尚处于起步阶段,仅见于少数访花昆虫或粪食性昆虫,建议加强以下几个方面的研究：(1)重大夜行性农业害虫的微光视觉及其应用的研究;(2)非典型重叠复眼的光学结构特征及其应对微光环境的适应机制研究;(3)夜行性昆虫响应微光环境的视觉适应机制研究;(4)基于夜行性昆虫微光视觉行为研发新型害虫防控技术。     

The Effect of Zeaxanthin on the Visual Acuity of Zebrafish

Oral supplementation of carotenoids such as zeaxanthin or lutein which naturally occur in human retina have been shown to improve vision and prevent progression of damage to advanced AMD in some studies. The zebrafish eye shares many physiological similarities with the human eye and is increasingly being used as model for vision research. We hypothesized that injection of zeaxanthin into the zebrafish eye would improve the visual acuity of the zebrafish over time. Visual acuity, calculated in cycles per degree, was measured in adult zebrafish to establish a consistent baseline using the optokinetic response. Zeaxanthin dissolved into phosphate buffered saline (PBS) or PBS only was injected into the anterior chamber of the right and left eyes of the Zebrafish. Visual acuities were measured at 1 week and 3, 8 and 12 weeks post-injection to compare to baseline values. Repeated measures ANOVA was used to compare visual acuities between fish injected with PBS and zeaxanthin. A significant improvement in visual acuity, 14% better than before the injection (baseline levels), was observed one week after injection with zeaxanthin (p = 0.04). This improvement peaked at more than 30% for some fish a few weeks after the injection and improvement in vision persisted at 3 weeks after injection (p = 0.006). The enhanced visual function was not significantly better than baseline at 8 weeks (p = 0.19) and returned to baseline levels 12 weeks after the initial injection (p = 0.50). Zeaxanthin can improve visual acuity in zebrafish eyes. Further studies are required to develop a better understanding of the role zeaxanthin and other carotenoids play during normal visual function.     

Manuo-ocular coordination in target tracking. II. Comparing the model with human behavior

Several studies have shown that humans track a moving visual target with their eyes better if the movement of this target is directly controlled by the observer's hand. The improvement in performance has been attributed to coordination control between the arm motor system and the smooth pursuit (SP) system. In such a task, the SP system shows characteristics that differ from those observed during eye-alone tracking: latency (between the target-arm and the eye motion onsets) is shorter, maximum SP velocity is higher and the maximum target motion frequency at which the SP can function effectively is also higher. The aim of this article is to qualitatively evaluate the behavior of a dynamical model simulating the oculomotor system and the arm motor system when both are involved in tracking visual targets. The evaluation is essentially based on a comparison of the behavior of the model with the behavior of human subjects tracking visual targets under different conditions. The model has been introduced and quantitatively evaluated in a companion paper. The model is based on an exchange of internal information between the two sensorimotor systems, mediated by sensory signals (vision, arm muscle proprioception) and motor signals (arm motor command copy). The exchange is achieved by a specialized structure of the central nervous system, previously identified as a part of the cerebellum. Computer simulation of the model yielded results that fit the behavior of human subjects observed during previously reported experiments, both qualitatively and quantitatively. The parallelism between physiology and human behavior on the one hand, and structure and simulation of the model on the other hand, is discussed. Received: 6 March 1997 / Accepted in revised form: 15 July 1997     

Using perturbations to identify the brain circuits underlying active vision

The visual and oculomotor systems in the brain have been studied extensively in the primate. Together, they can be regarded as a single brain system that underlies active vision—the normal vision that begins with visual processing in the retina and extends through the brain to the generation of eye movement by the brainstem. The system is probably one of the most thoroughly studied brain systems in the primate, and it offers an ideal opportunity to evaluate the advantages and disadvantages of the series of perturbation techniques that have been used to study it. The perturbations have been critical in moving from correlations between neuronal activity and behaviour closer to a causal relation between neuronal activity and behaviour. The same perturbation techniques have also been used to tease out neuronal circuits that are related to active vision that in turn are driving behaviour. The evolution of perturbation techniques includes ablation of both cortical and subcortical targets, punctate chemical lesions, reversible inactivations, electrical stimulation, and finally the expanding optogenetic techniques. The evolution of perturbation techniques has supported progressively stronger conclusions about what neuronal circuits in the brain underlie active vision and how the circuits themselves might be organized.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Electrical Stimulation of the Shark Brain

Early studies using various means to electrically activate portionsof the brain in immobilized elasmobranchs are critically reviewed.The results of brain stimulation experiments using modern techniquesare then considered in light of this background material. Preliminaryexperiments on anesthetized-immobilized sharpnose and bonnetheadsharks are given as an outline of the types of responses thatcan be studied using acute preparations of pelagic sharks. Theresponses evoked can be grouped into the following categories:arousal and swimming; body, fin and eye movements suggestiveof circling and loss of equilibrium; possible components ofagonistic and reproductive behavior; head, mouth and respiratorymovements and possible color changes. Chronic studies on free-swimmingsharpnose sharks are discussed with respect to potential areasfor future study. Responses suggestive of portions of agonisticand feeding behavior were evoked but no attempt was made tolocalize the areas stimulated. The behavioral effects of electricalstimulation of 85 electrodes in free-swimming juvenile nursesharks are presented in some detail. The anatomical distributionof sites from which the following responses have been elicitedare plotted on representative sections of the brain: arousalescape;coughing; head shaking; barbel movement; eye retraction; bitingor mouthing food; snapping up gravel; slow dragging of the barbelsacross the substrate; circling; rolling about the long axis;continuous swimming and interrupted swimming. Several possiblefunctional-anatomical systems are suggested to account for someof these results.     

The two axes of the human eye and inversion of the retinal layers: The basis for the interpretation of the retina as a phase grating optical,cellular 3D chip

The question of why the human eye has two axes, a photopic visual axis, and an eye axis, is just as justified as the one of why the fovea is not on the eye axis, but instead is on the visual axis. An optical engineer would have omitted the second axis and placed the fovea on the eye axis. The answer to the question of why the design of the real eye differs from the logic of the engineer is found in its prenatal development. The biaxial structure was the only possible consequence of the decision to invert the retinal layers. Accordingly, this is of considerable importance. It, in turn, forms the basis of the interpretation of the retina as a cellular 3D phase grating, and can provide a grating-optical interpretation of adaptive effects (Purkinje shift) and aperture phenomena (Stiles-Crawford effects I and II, Bezold-Brücke phenomenon) and visual acuity data in photopic and scotopic vision.     

Energy conservation characterizes sleep in sharks

Sharks represent the earliest group of jawed vertebrates and as such, they may provide original insight for understanding the evolution of sleep in more derived animals. Unfortunately, beyond a single behavioural investigation, very little is known about sleep in these ancient predators. As such, recordings of physiological indicators of sleep in sharks have never been reported. Reduced energy expenditure arising from sustained restfulness and lowered metabolic rate during sleep have given rise to the hypothesis that sleep plays an important role for energy conservation. To determine whether this idea applies also to sharks, we compared metabolic rates of draughtsboard sharks (Cephaloscyllium isabellum) during periods ostensibly thought to be sleep, along with restful and actively swimming sharks across a 24 h period. We also investigated behaviours that often characterize sleep in other animals, including eye closure and postural recumbency, to establish relationships between physiology and behaviour. Overall, lower metabolic rate and a flat body posture reflect sleep in draughtsboard sharks, whereas eye closure is a poorer indication of sleep. Our results support the idea for the conservation of energy as a function of sleep in these basal vertebrates.     

Review of children referred from the school vision screening programme in Kettering during 1976-8.

The progress of 108 children who were identified by the vision screening programme in school as having defective vision (excluding those with puberty onset myopia) was reviewed. Treatment of these children resulted in improvement in visual acuity of the worst eye (two lines or better) for 16 children. Eighteen children had severe amblyopia (6/24 or worse). Among these the vision of only five was improved by treatment. Two thirds of the children had refractive errors in the better eye which required correction. It seems sensible to identify and treat children with bilateral refractive errors, but the need to treat children with lesser degrees of amblyopia is questioned.     

Visual system of the stalk-eyed fly,Cyrtodiopsis quinqueguttata (Diopsidae,Diptera): an anatomical investigation of unusual eyes

Diopsid flies have eye stalks up to a centimeter in length, displacing the retina laterally from the rest of the head. This bizarre condition, called hypercephaly, is rare, but has evolved independently among several insect orders and is most common in flies (Diptera). Earlier studies of geometrical optics and behavior have led to various hypotheses about possible adaptive advantages of eye stalks, such as enhanced stereoscopic vision while other hypothesis suggest that eye stalks are an outcome of sexual selection. Here, we focus on how these curious distortions of head/eye morphology are accompanied by changes in the neural organization of the visual system of Cyrtodiopsis quinqueguttata. Histological examinations reveal that the optic lobes, lamina (La), medulla (Me), lobula (Lo), and lobula plate (LP) are contained entirely within the fly's eye bulbs, which are located at the distal ends of the eye stalks. We report that the organization of the peripheral visual system (La and Me) is similar to that of other Diptera (e.g., Musca and Drosophila), but deeper visual areas (Lo and LP) have been more strongly modified. For example, in both the lobula and lobula plate, fewer but larger giant collector neurons are found. The most pronounced difference is the reduction in the number of wide-field vertical cells of the lobula plate, where there are only four relatively large fibers, as opposed to 11 in Musca. The “fewer but larger” neural organization may enhance the conduction velocities of these cells, but may result in a loss of spatial resolution. At the base of the eye bulb, axon bundles collect and form a long optic nerve that extends the length of the eye stalk. We suggest that this organization of the diopsid visual system provides evidence for the costs of possessing long eye stalks. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 449–468, 1998     

Homeostasis of eye growth and the question of myopia

As with other organs, the eye's growth is regulated by homeostatic control mechanisms. Unlike other organs, the eye relies on vision as a principal input to guide growth. In this review, we consider several implications of this visual guidance. First, we compare the regulation of eye growth to that of other organs. Second, we ask how the visual system derives signals that distinguish the blur of an eye too large from one too small. Third, we ask what cascade of chemical signals constitutes this growth control system. Finally, if the match between the length and optics of the eye is under homeostatic control, why do children so commonly develop myopia, and why does the myopia not limit itself? Long-neglected studies may provide an answer to this last question.     

Musca domestica inspired machine vision sensor with hyperacuity

A fiber optic sensor inspired by the compound eye of the common housefly, Musca domestica, has been developed. The sensor coupled with analog preprocessing hardware has the potential to extract edge information quickly and in parallel. The design is motivated by the parallel nature of the fly's vision system and its demonstrated hyperacuity or precision of visual localization beyond the conventional resolution limit. The fly's anatomy supporting the design is reviewed, followed by the design of a one-dimensional, cartridge-based sensor. The sensor's ability to locate a line stimulus in a two-dimensional space is demonstrated. Discussion is provided to extend this work in scale, cartridge dimension, information and array processing.     

Eye movements modulate visual receptive fields of V4 neurons

The receptive field, defined as the spatiotemporal selectivity of neurons to sensory stimuli, is central to our understanding of the neuronal mechanisms of perception. However, despite the fact that eye movements are critical during normal vision, the influence of eye movements on the structure of receptive fields has never been characterized. Here, we map the receptive fields of macaque area V4 neurons during saccadic eye movements and find that receptive fields are remarkably dynamic. Specifically, before the initiation of a saccadic eye movement, receptive fields shrink and shift towards the saccade target. These spatiotemporal dynamics may enhance information processing of relevant stimuli during the scanning of a visual scene, thereby assisting the selection of saccade targets and accelerating the analysis of the visual scene during free viewing.     

Seeing the light: new insights into the molecular pathogenesis of retinal diseases

In the past, most treatments for retinal diseases have been empirical. Steroids and/or laser photocoagulation and/or surgery have been tried for almost every condition with little or no understanding of the underlying disease. Over the past several years vision researchers have uncovered molecular components of processes, such as visual transduction and the visual cycle, that are critical for visual function, and identified other molecules that lead to dysfunction and disease processes such as neovascularization and macular edema. It is becoming clear that dysregulation of certain molecules can have major effects on retinal structure and function. Studies in animal models have suggested that inhibiting or augmenting levels of a single molecule can have major effects in complex disease processes. Although several molecules probably contribute to neovascularization and excessive vascular permeability in the eye, blockade of vascular endothelial growth factor (VEGF) has remarkable beneficial effects in animal models that have now been proven to apply to human diseases in clinical trials. Intraocular injection of VEGF antagonists has revolutionized the treatment of choroidal neovascularization (CNV) and macular edema and serves as a model of targeted ocular pharmacotherapy. Significant progress elucidating the molecular pathogenesis of several disease processes in the eye may soon lead to new treatments following the lead of VEGF antagonists. Initial treatments that provide benefit from frequent intraocular injections are likely to be followed by sustained delivery of drugs and/or prolonged protein delivery by gene transfer. The eye has entered the era of molecular therapy.     

The architecture of visual cortex and inferential processes in vision

This paper is organised approximately into two halves. In the first half, I review evidence about the structure of the visual system, and I use that evidence to frame what I think are widely held but often implicit ideas about how it works, namely that vision is principally analysis of retinal input. These ideas have been strongly influenced by engineering approaches; form a default view of the visual system that suffuses all the language used to describe it (at least in visual neuroscience); and are to some extent supported by the structural evidence. In the second half, I explore some inconvenient facts from neuroanatomy and neurophysiology which are quite uncomfortable for the traditional view. I then set out a contrary view of how structure and function are linked in the visual system, which is a neurobiological variety of the quite developed view in psychophysics that vision is better understood as knowledge-rich inference. Finally, I explore some of the ramifications of this view for neurophysiological understanding of how the visual system might operate during normal vision.