The Evolution of Gaze Shifting Eye Movements.

In animals with good eyesight most eye movements consist of saccades, which rapidly shift the direction of the eye's axis, and intervals between the saccades (fixations) in which gaze is kept stationary relative to the surroundings. This stability is needed to prevent motion blur, and it is achieved by reflexes which counter-rotate the eye when the head moves. This saccade-and-fixate strategy arose early in fish evolution, when the original function of saccades was to re-centre the eye as the fish turned. In primates, and other foveate vertebrates, saccades took on the new function of directing the fovea to objects of interest in the surroundings. Among invertebrates the same saccade-and-fixate pattern is seen, especially in insects, crustaceans and cephalopod molluscs.

Arthropod eyes: The early Cambrian fossil record and divergent evolution of visual systems.

Four types of eyes serve the visual neuropils of extant arthropods: compound retinas composed of adjacent facets; a visual surface populated by spaced eyelets; a smooth transparent cuticle providing inwardly directed lens cylinders; and single-lens eyes. The first type is a characteristic of pancrustaceans, the eyes of which comprise lenses arranged as hexagonal or rectilinear arrays, each lens crowning 8-9 photoreceptor neurons. Except for Scutigeromorpha, the second type typifies Myriapoda whose relatively large eyelets surmount numerous photoreceptive rhabdoms stacked together as tiers. Scutigeromorph eyes are facetted, each lens crowning some dozen photoreceptor neurons of a modified apposition-type eye. Extant chelicerate eyes are single-lensed except in xiphosurans, whose lateral eyes comprise a cuticle with a smooth outer surface and an inner one providing regular arrays of lens cylinders. This account discusses whether these disparate eye types speak for or against divergence from one ancestral eye type. Previous considerations of eye evolution, focusing on the eyes of trilobites and on facet proliferation in xiphosurans and myriapods, have proposed that the mode of development of eyes in those taxa is distinct from that of pancrustaceans and is the plesiomorphic condition from which facetted eyes have evolved. But the recent discovery of enormous regularly facetted compound eyes belonging to early Cambrian radiodontans suggests that high-resolution facetted eyes with superior optics may be the ground pattern organization for arthropods, predating the evolution of arthrodization and jointed post-protocerebral appendages. Here we provide evidence that compound eye organization in stem-group euarthropods of the Cambrian can be understood in terms of eye morphologies diverging from this ancestral radiodontan-type ground pattern. We show that in certain Cambrian groups apposition eyes relate to fixed or mobile eyestalks, whereas other groups reveal concomitant evolution of sessile eyes equipped with optics typical of extant xiphosurans. Observations of fossil material, including that of trilobites and eurypterids, support the proposition that the ancestral compound eye was the apposition type. Cambrian arthropods include possible precursors of mandibulate eyes. The latter are the modified compound eyes, now sessile, and their underlying optic lobes exemplified by scutigeromorph chilopods, and the mobile stalked compound eyes and more elaborate optic lobes typifying Pancrustacea. Radical divergence from an ancestral apposition type is demonstrated by the evolution of chelicerate eyes, from doublet sessile-eyed stem-group taxa to special apposition eyes of xiphosurans, the compound eyes of eurypterids, and single-lens eyes of arachnids. Different eye types are discussed with respect to possible modes of life of the extinct species that possessed them, comparing these to extant counterparts and the types of visual centers the eyes might have served.

Eye and head movements shape gaze shifts in Indian peafowl.

Animals selectively direct their visual attention toward relevant aspects of their environments. They can shift their attention using a combination of eye, head and body movements. While we have a growing understanding of eye and head movements in mammals, we know little about these processes in birds. We therefore measured the eye and head movements of freely behaving Indian peafowl (Pavo cristatus) using a telemetric eye-tracker. Both eye and head movements contributed to gaze changes in peafowl. When gaze shifts were smaller, eye movements played a larger role than when gaze shifts were larger. The duration and velocity of eye and head movements were positively related to the size of the eye and head movements, respectively. In addition, the coordination of eye and head movements in peafowl differed from that in mammals; peafowl exhibited a near-absence of the vestibulo-ocular reflex, which may partly result from the peafowl's ability to move their heads as quickly as their eyes.

Eye movements of vertebrates and their relation to eye form and function.

The types of eye movements shown by all vertebrates originated in the earliest fishes. These consisted of compensatory movements, both vestibular and visual, to prevent image motion, and saccades to relocate gaze. All vertebrates fixate food items with their heads to enable ingestion, but from teleosts onwards some species also use eye movements to target particular objects, especially food. Eye movement use is related to the resolution distribution in the retina, with eyes that contain foveas, or areas of high ganglion cell density, being more likely to make targeting eye movements, not seen in animals with more uniform retinas. Birds, in particular, tend mainly to use head movements when shifting gaze. Many birds also make translatory head saccades (head bobbing) when walking. It is common for animals to use both eyes when locating food items ahead, but the use of binocular disparity for distance judgment is rare, and has only been demonstrated in toads, owls, cats and primates. Smooth tracking with eyes alone is probably confined to primates. The extent of synchrony and directional symmetry in the movements of the two eyes varies greatly, from complete independence in the sandlance and chameleon, to perfect coordination in primates.

Animal vision: starfish can see at last.

Starfish have small compound eyes at the ends of their arms. Until recently no behavioural function had been found for them, but now it appears that starfish are able to use them to navigate to the edges of reefs from which they sometimes stray.

On the eyes of male coffee berry borers as rudimentary organs.

The coffee berry borer, Hypothenemus hampei, is the most damaging insect pest of coffee worldwide. Like males in other species in the genus, male coffee berry borers have a lower number of facets in the compound eyes than females. The rudimentary eyes in male coffee berry borers could be an evolutionary response to their cryptic life habit, whereby they are born inside a coffee berry and never leave the berry. The main objective of the study was to determine if the differences in the number of facets translates into differences in visual acuity. We used low-temperature scanning electron microscopy to visualize and quantify the number of facets in the compound eyes. There was a significantly lower (p<0.0001) number of facets in males (19.1 ± 4.10) than in females (127.5 ± 3.88). To assess visual acuity, we conducted optomotor response experiments, which indicate that females respond to movement, while males did not respond under the conditions tested. The coffee berry borer is an example of an insect whereby disuse of an organ has led to a rudimentary compound eye. This is the first study that has experimentally tested responses to movement in bark beetles.

Do we have an internal model of the outside world?

Our phenomenal world remains stationary in spite of movements of the eyes, head and body. In addition, we can point or turn to objects in the surroundings whether or not they are in the field of view. In this review, I argue that these two features of experience and behaviour are related. The ability to interact with objects we cannot see implies an internal memory model of the surroundings, available to the motor system. And, because we maintain this ability when we move around, the model must be updated, so that the locations of object memories change continuously to provide accurate directional information. The model thus contains an internal representation of both the surroundings and the motions of the head and body: in other words, a stable representation of space. Recent functional MRI studies have provided strong evidence that this egocentric representation has a location in the precuneus, on the medial surface of the superior parietal cortex. This is a region previously identified with 'self-centred mental imagery', so it seems likely that the stable egocentric representation, required by the motor system, is also the source of our conscious percept of a stable world.

Animal vision: rats watch the sky.

A recent study using two head-mounted cameras has found that, in freely moving rats, eye movements are usually not conjugate, precluding stereopsis, but they maintain a wide region of binocular overlap above the head, presumably to detect flying predators.

The evolution of lenses.

Structures which bend light and so form images are present in all the major phyla. Lenses with a graded refractive index, and hence reduced spherical aberration, evolved in the vertebrates, arthropods, annelid worms, and several times in the molluscs. Even cubozoan jellyfish have lens eyes. In some vertebrate eyes, multiple focal lengths allow some correction for chromatic aberration. In land vertebrates the cornea took over the main ray-bending task, leaving accommodation as the main function of the lens. The spiders are the only other group to make use of a single cornea as the optical system in their main eyes, and some of these - the salticids - have evolved a remarkable system based on image scanning. Similar scanning arrangements are found in some crustaceans, sea-snails and insect larvae.

The operation of the visual system in relation to action.

Neurophysiologists studying the visual representation of the world in the parietal lobe generally find that it is based in a gaze-centred (retinotopic) frame. Students of orientation, however, find that the brain also contains a more panoramic egocentric representation that allows appropriate motor actions to take place independent of the orientation of the eyes and head. This representation can operate temporarily without visual input, but is updated from the vestibular system and from other modalities. In this minireview, I shall consider how these two representations are kept aligned with each other, and how they relate to the organisation of motor actions and to the phenomenal world that we see.

Marine optics: dark disguise.

Survival in the deep sea depends on seeing others without being seen yourself. A recent study examined two switchable camouflage strategies in cephalopods: transparency and dark pigmentation.

Eye guidance in natural vision: reinterpreting salience.

Models of gaze allocation in complex scenes are derived mainly from studies of static picture viewing. The dominant framework to emerge has been image salience, where properties of the stimulus play a crucial role in guiding the eyes. However, salience-based schemes are poor at accounting for many aspects of picture viewing and can fail dramatically in the context of natural task performance. These failures have led to the development of new models of gaze allocation in scene viewing that address a number of these issues. However, models based on the picture-viewing paradigm are unlikely to generalize to a broader range of experimental contexts, because the stimulus context is limited, and the dynamic, task-driven nature of vision is not represented. We argue that there is a need to move away from this class of model and find the principles that govern gaze allocation in a broader range of settings. We outline the major limitations of salience-based selection schemes and highlight what we have learned from studies of gaze allocation in natural vision. Clear principles of selection are found across many instances of natural vision and these are not the principles that might be expected from picture-viewing studies. We discuss the emerging theoretical framework for gaze allocation on the basis of reward maximization and uncertainty reduction.

Animal eyes: defending the coat of mail.

The eyes on the backs of molluscs known as chitons are shadow and motion detectors, the lenses of which are made of birefringent aragonite. These provide a focus both in and out of water.

Vision and the representation of the surroundings in spatial memory.

One of the paradoxes of vision is that the world as it appears to us and the image on the retina at any moment are not much like each other. The visual world seems to be extensive and continuous across time. However, the manner in which we sample the visual environment is neither extensive nor continuous. How does the brain reconcile these differences? Here, we consider existing evidence from both static and dynamic viewing paradigms together with the logical requirements of any representational scheme that would be able to support active behaviour. While static scene viewing paradigms favour extensive, but perhaps abstracted, memory representations, dynamic settings suggest sparser and task-selective representation. We suggest that in dynamic settings where movement within extended environments is required to complete a task, the combination of visual input, egocentric and allocentric representations work together to allow efficient behaviour. The egocentric model serves as a coding scheme in which actions can be planned, but also offers a potential means of providing the perceptual stability that we experience.

Fairground rides and spatial updating.

A simple experiment with a rotating office chair demonstrates that the extent of counter-rotation we experience when imposed rotation has stopped is the same as the angular inaccuracy of pointing to a previously fixated object. This suggests that our conscious percept of rotation and the updating signal for the egocentric model we use to guide motor actions are closely related.

Vision, eye movements, and natural behavior.

Historically, the principal function of vision has been to provide the information needed to support action. Visually mediated actions rely on three systems: the gaze system responsible for locating and fixating task-relevant objects, the motor system of the limbs to carry out the task, and the visual system to supply information to the other two. All three systems are under the control of a fourth system, the schema system, which specifies the current task and plans the overall sequence of actions. These four systems have separate but interconnected cortical representations. The way these systems interact in time and space is discussed here in relation to two studies of the gaze changes and manipulations made during two ordinary food preparation tasks. The main conclusions are that complex action sequences consist of a succession of individual object-related actions, each of which typically involve a turn toward the object (if needed), followed by fixation and finally manipulation monitored by vision. Gaze often moves on to the next object just before manipulation is complete. Task-irrelevant objects are hardly ever fixated, implying that the control of fixation comes principally from top-down instructions from the schema system, not bottom-up salience. Single fixations have identifiable functions (locating, directing, guiding, and checking) related to the action to be taken. Several variants of the basic object-related action scheme are discussed, including single-action events in ball sports involving only one anticipatory gaze shift, continuous production loops in text and music reading, and storage-action alternation in copying tasks such as portrait sketching.

Biological optics: deep reflections.

An image-forming optical system that is based on a mirror with an unconventional structure has recently been discovered in a deep-sea fish.

Optics of the ultraviolet reflecting scales of a jumping spider.

The jumping spider Cosmophasis umbratica from Singapore is strongly sexually dimorphic. The males, but not the females, reflect ultraviolet as well as green-orange light. The scales responsible for this are composed of a chitin-air-chitin sandwich in which the chitin layers are three-quarters of a wavelength thick and the air gap a quarter wavelength (where lambda=600 nm, the peak wavelength of the principal reflection maximum). It is shown that this configuration produces a second reflectance peak at approximately 385 nm, accounting for the observed reflection in the ultraviolet. Other scales have a similar thickness of chitin but lack the air gap and thus produce a dull purple reflection. This novel mechanism provides the spiders with two colour signals, both of which are important in mating displays.

Sex-specific UV and fluorescence signals in jumping spiders.

No animals are known to possess both ultraviolet (UV) reflectance and fluorescence that are sex-specific. We provide evidence for this separation in the jumping spider Cosmophasis umbratica, which has UV reflectance and UV-induced green fluorescence restricted to males and females, respectively. During courtship, many of the studied pairs failed to show typical display posturing when UV light was blocked. Occluding the UV component of sunlight to only one of each pair also caused atypical behavior: Females showed no interest in non-UV-reflective courting males, and males either ignored or were lackluster in courting nonfluorescing females. These results demonstrate the importance of both sex-specific hues as sexual signals for effective intraspecific communication.