Motion and vision: why animals move their eyes

Nearly all animals with good vision have a repertoire of eye movements. The majority show a pattern of stable fixations with fast saccades that shift the direction of gaze. These movements may be made by the eyes themselves, or the head, or in some insects the whole body. The main reason for keeping gaze still during fixations is the need to avoid the blur that results from the long response time of the photoreceptors. Blur begins to degrade the image at a retinal velocity of about 1 receptor acceptance angle per response time. Some insects (e.g. hoverflies) stabilise their gaze much more rigidly than this rule implies, and it is suggested that the need to see the motion of small objects against a background imposes even more stringent conditions on image motion. A third reason for preventing rotational image motion is to prevent contamination of the translational flow-field, by which a moving animal can judge its heading and the distances of objects. Some animals do let their eyes rotate smoothly, and these include some heteropod molluscs, mantis shrimps and jumping spiders, all of which have narrow linear retinae which scan across the surroundings. Hymenopteran insects also rotate during orientation flights at speeds of 100–200° s⁻¹. This is just consistent with a blur-free image, as are the scanning speeds of the animals with linear retinae. Accepted: 29 April 1999     

Object motion: a world view

Moving objects are detected by virtue of their shifting image on the retina. But to know how objects are moving in the world, we must take into account the rotation of our eyes, as well as the rotation of our head. A recent paper describes neurons that carry out this computation.     

What are birds looking at? Head movements and eye use in chickens

Using video recordings of hens, Gallus gallus domesticus, as they approached different kinds of objects, I examined how change in object distance is associated with a change from lateral to binocular viewing. The birds tended to view distant objects laterally while they preferentially viewed objects less than 20-30 cm away frontally; this was true whether they were looking at another bird or at an inanimate object. However, as well as switching between lateral and frontal viewing, the hens also swung their heads from side to side with movements so large that the same object appeared to be viewed with completely different parts of the retina, and even with different eyes, in rapid succession. When confronted with a novel object, the hens walked more slowly but continued to show large head movements. This suggests that, unlike mammals, which gaze fixedly at novel objects, hens investigate them by moving the head and looking at them with different, specialized, parts of their eyes. Many aspects of bird behaviour, such as search image formation, vigilance and visual discriminations, may be affected by the way they move the head and eyes. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Freely flying bees discriminate between stationary and moving objects: performance and possible mechanisms

Summary Freely flying honeybees are innately attracted to moving objects, as revealed by their spontaneous preference for a moving disc over an identical, but stationary disc. We have exploited this spontaneous preference to explore the visual cues by which a bee, which is herself in motion, recognizes a moving object. We find that the moving disc is not detected on the basis that it produces a more rapidly moving image on the retina. The relevant cue might therefore be the motion of the disc relative to the visual surround. We have attempted to test this hypothesis by artificially rotating the structured environment, together with the moving disc, around the bee. Under these conditions, the image of the stationary disc rather than that of the actually moving disc is in motion relative to the surround. We find that rotation of the surround disrupts the bee's capacity not only to distinguish a moving object from a stationary one, but also to discriminate stationary objects at different ranges. Possible interpretations of these results are discussed.     

Posterior parietal cortex neurons encode target motion in world-centered coordinates

The motion areas of posterior parietal cortex extract information on visual motion for perception as well as for the guidance of movement. It is usually assumed that neurons in posterior parietal cortex represent visual motion relative to the retina. Current models describing action guided by moving objects work successfully based on this assumption. However, here we show that the pursuit-related responses of a distinct group of neurons in area MST of monkeys are at odds with this view. Rather than signaling object image motion on the retina, they represent object motion in world-centered coordinates. This representation may simplify the coordination of object-directed action and ego motion-invariant visual perception.     

Human visual system integrates color signals along a motion trajectory

Whether fundamental visual attributes, such as color, motion, and shape, are analyzed separately in specialized pathways has been one of the central questions of visual neuroscience. Although recent studies have revealed various forms of cross-attribute interactions, including significant contributions of color signals to motion processing, it is still widely believed that color perception is relatively independent of motion processing. Here, we report a new color illusion, motion-induced color mixing, in which moving bars, the color of each of which alternates between two colors (e.g., red and green), are perceived as the mixed color (e.g., yellow) even though the two colors are never superimposed on the retina. The magnitude of color mixture is significantly stronger than that expected from direction-insensitive spatial integration of color signals. This illusion cannot be ascribed to optical image blurs, including those induced by chromatic aberration, or to involuntary eye movements of the observer. Our findings indicate that color signals are integrated not only at the same retinal location, but also along a motion trajectory. It is possible that this neural mechanism helps us to see veridical colors for moving objects by reducing motion blur, as in the case of luminance-based pattern perception.     

Synchronized firing among retinal ganglion cells signals motion reversal

We show that when a moving object suddenly reverses direction, there is a brief, synchronous burst of firing within a population of retinal ganglion cells. This burst can be driven by either the leading or trailing edge of the object. The latency is constant for movement at different speeds, objects of different size, and bright versus dark contrasts. The same ganglion cells that signal a motion reversal also respond to smooth motion. We show that the brain can build a pure reversal detector using only a linear filter that reads out synchrony from a group of ganglion cells. These results indicate that not only can the retina anticipate the location of a smoothly moving object, but that it can also signal violations in its own prediction. We show that the reversal response cannot be explained by models of the classical receptive field and suggest that nonlinear receptive field subunits may be responsible.     

Visuomotor Response to Object Expansion in Free-Flying Bumble Bees

The flight control systems of flying insects enable many kinds of sophisticated maneuvers, including avoidance of midair collisions. Visuomotor response to an approaching object, received as image expansion on insects’ retina, is a complex event in a dynamic environment where both animals and objects are moving. There are intensive free flight studies on the landing response in which insects receive image expansion by their own movement. However, few studies have been conducted regarding how freely flying insects respond to approaching objects. Here, using common laboratory insects for behavioral research, the bumblebee Bombus ignitus, we examined their visual response to an approaching object in the free-flying condition. While the insect was slowly flying in a free-flight arena, an expanding stripe was projected laterally from one side of the arena with a high-speed digital mirror device projector. Rather than turning away reported before, the bumble bees performed complex flight maneuvers. We synchronized flight trajectories, orientations and wing stroke frequencies with projection parameters of temporal resolution in 0.5 ms, and analyzed the instantaneous relationship between visual input and behavioral output. In their complex behavioral responses, we identified the following two visuomotor behaviors: increasing stroke frequency when the bumble bees confront the stripe expansion, and turning towards (not away) the stripe expansion when it is located laterally to the bee. Our results suggested that the response to object expansion is not a simple and reflexive escape but includes object fixation, presumably for subsequent behavioral choice.     

Vision: Visual space is not what it appears to be

The location of visual objects in the world around us is reconstructed in a complex way from the image falling on the retina. Recent studies have begun to reveal the different ways in which the brain dynamically re-maps retinal information across eye movements to compute object locations for perception and directing actions.     

Parallel processing in the mammalian retina

Our eyes send different 'images' of the outside world to the brain - an image of contours (line drawing), a colour image (watercolour painting) or an image of moving objects (movie). This is commonly referred to as parallel processing, and starts as early as the first synapse of the retina, the cone pedicle. Here, the molecular composition of the transmitter receptors of the postsynaptic neurons defines which images are transferred to the inner retina. Within the second synaptic layer - the inner plexiform layer - circuits that involve complex inhibitory and excitatory interactions represent filters that select 'what the eye tells the brain'.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

Elegant‐crested Tinamous Eudromia elegans do not synchronize head and leg movements during head‐bobbing

Head‐bobbing is the fore–aft movement of the head relative to the body during terrestrial locomotion in birds. It is considered to be a behaviour that helps to stabilize images on the retina during locomotion, yet some studies have suggested biomechanical links between the movements of the head and legs. This study analysed terrestrial locomotion and head‐bobbing in the Elegant‐crested Tinamou Eudromia elegans at a range of speeds by synchronously recording high‐speed video and ground reaction forces in a laboratory setting. The results indicate that the timing of head and leg movements are dissociated from one another. Nonetheless, head and neck movements do affect stance duration, ground reaction forces and body pitch and, as a result, the movement of the centre of mass in head‐bobbing birds. This study does not support the hypothesis that head‐bobbing is itself constrained by terrestrial locomotion. Instead, it suggests that visual cues are the primary trigger for head‐bobbing in birds, and locomotion is, in turn, constrained by a need for image stabilization and depth perception.     

Visual receptive field properties of feature detecting neurons in the dragonfly

The dragonfly, (Aeshna, Anax) which feeds on small flying insects, requires a visual system capable of signaling the movements of airborne prey. A group of 8 descending feature detectors in the dragonfly are tuned exclusively to moving contrasting objects. These target-selective descending neurons project from the brain to the thoracic ganglia. Their activity drives steering movement of the wings.In this study, we recorded target-selective descending neuron activity intracellularly.To define their receptive fields, we recorded responses to the movement of black square targets projected onto a screen in front of the animal. Each neuron was identified by dye injection.Target-selective descending neurons exhibit several receptive field properties. Our results show that they are strongly directionally selective. Two TSDNs, exclusively tuned to small targets, have receptive fields restricted to visual midline. Others, which are not selective for target size, have asymmetric receptive fields centered laterally.We suggest that the behavioral function of these specialized feature detectors is to steer the dragonfly during prey-tracking so as to fix the position of the prey image on the retina. If the dragonfly maintains a constant visual bearing to its prey over time it will intercept its prey.Abbreviations TSDN target-selective descending neuron - DCMD descending contralateral movement detector - MDT median dorsal tract - DIT dorsal intermediate tract - VNC ventral nerve cord     

High school and college baseball pitchers response and glove movements to line drives

The timing of glove movements used by baseball pitchers to catch fast approaching balls (i.e., line drives) was examined in two tests to determine the responses and temporal characteristics of glove movements in high school and college baseball pitchers. Balls were projected toward the head of participants at 34.8 m.s-1 (78 mph) on average in an indoor test and at speeds approaching 58.1 m.s-1 (130 mph) in a field test. Pitchers caught over 80% and 15% of the projected balls in the indoor and field tests, respectively. Analyses of glove responses indicated that all pitchers could track the line drives and produce coordinated glove movements, which were initiated 160 ms (+/-47.8), on average, after the ball was launched. College pitchers made initial glove movements sooner than high school pitchers in the field test (p=0.012). In contrast, average glove velocity for pitchers increased from 1.33 (+/-0.61) to 3.45 (+/-0.86) m.s-1 across the tests, but did not differ between experience levels. Glove movement initiation and speed were unrelated, and pitchers utilized visual information throughout the ball's flight to catch balls that approached at speeds exceeding the estimated speeds in competitive situations.     

Real time computer tracking of free-swimming and tethered rotating cells

A computerized image processing system has been developed that tracks individual free-swimming cells and rotating bacterial cell bodies tethered by their flagella in real time. Free-swimming bacteria of Rhodobacter sphaeroides, Rhodospirullum rubrum, and Salmonella typhimurium have been tracked swimming at speeds from 0 to over 120 microns s-1. A high level of discrimination is exerted against noncellular objects, allowing analysis of stopped as well as moving cells. This enabled detection of both speed and qualitative change in the swimming patterns of R. sphaeroides WS8 upon tactic stimulation. Comparison with darkfield microscopy indicated that the two techniques were in substantial agreement. The unidirectional rotation of cells of R. sphaeroides WS8 could be detected when the cells were either parallel to the microscope slide or end on. Frequencies of rotation of up to 10 Hz were monitored before image blurring became a problem. True rods would be easier to analyze at higher speeds of rotation. Although developed for photosynthetic bacteria, a wide range of bacteria, eucaryotic organisms, and subcellular organelles could be tracked with this system. Minor modifications to the software allow customization to different types of motility analysis.     

Peripheral electrosensory imaging by weakly electric fish

Different species have developed different solutions to the problem of constructing a representation of the environment from sensory images projected onto sensory surfaces. Comprehension of how these images are formed is an essential first step in understanding the representation of external reality by a given sensory system. Modeling of the electrical sensory images of objects began with the discovery of electroreception and continues to provide general insights into the mechanisms of imaging. Progress in electric image research has made it possible to establish the physical basis of electric imaging, as well as methods to accurately predict the electric images of objects alone and as a part of a natural electric scene. In this review, we show the following. (1) The internal low resistance of the fish’s body shapes the image in two different ways: by funneling the current generated by the electric organ to the sensory surface, it increases the fields rostrally, thus enhancing the perturbation produced by nearby objects; and by increasing the projected image. (2) The electric fish’s self-generated currents are modified by capacitive objects in a distinctive manner. These modulations can be detected by different receptor types, yielding the possibility of “electric color.” (3) The effects of different objects in a scene interact with each other, generating an image that is different from the simple addition of the images of individual objects, thus causing strong contextual effects.     

Perceiving spatial relations via attentional tracking and shifting

Perceiving which of a scene's objects are adjacent may require selecting them with a limited-capacity attentional process. Previous results support this notion [1-3] but leave open whether the process operates simultaneously on several objects or proceeds one by one. With arrays of colored discs moving together, we first tested the effect of moving the discs faster than the speed limit for following them with attentional selection [4]. At these high speeds, participants could identify which colors were present and determine whether identical arrays were aligned or offset by one disc. They could not, however, apprehend which colors in the arrays were adjacent, indicating that attentional selection is required for this judgment. If selection operates serially to determine which colors are neighbors, then after the color of one disc is identified, attention must shift to the adjacent disc. As a result of the motion, attention might occasionally miss its target and land on the trailing disc. We cued attention to first select one or the other of a pair of discs and found the pattern of errors predicted. Perceiving these spatial relationships evidently requires selecting and processing objects one by one and is only possible at low object speeds.     

The role of background movement in goldfish vision

In experiments described in the literature objects presented to restrained goldfish failed to induce eye movements like fixation and/or tracking. We show here that eye movements can be induced only if the background (visual surround) is not stationary relative to the fish but moving. We investigated the influence of background motion on eye movements in the range of angular velocities of 5–20° s⁻¹. The response to presentation of an object is a transient shift in mean horizontal eye position which lasts for some 10 s. If an object is presented in front of the fish the eyes move in a direction such that it is seen more or less symmetrically by both eyes. If it is presented at ±70° from the fish's long axis the eye on the side of the object moves in the direction that the object falls more centrally on its retina. During these object induced eye responses the typical optokinetic nystagmus of amplitude of some 5° with alternating fast and slow phases is maintained, and the eye velocity during the slow phase is not modified by presentation of the object. Presenting an object in front of stationary or moving backgrounds leads to transient suppression of respiration which shows habituation to repeated object presentations. Accepted: 14 April 2000     

Gaze control: role of the parietal cortex

Eye movements constitute one of the most basic means of interacting with our environment, allowing to orient to, localize and scrutinize the variety of potentially interesting objects that surround us. In this review we discuss the role of the parietal cortex in the control of saccadic and smooth pursuit eye movements, whose purpose is to rapidly displace the line of gaze and to maintain a moving object on the central retina, respectively. From single cell recording studies in monkey we know that distinct sub-regions of the parietal lobe are implicated in these two kinds of movement. The middle temporal (MT) and medial superior temporal (MST) areas show neuronal activities related to moving visual stimuli and to ocular pursuit. The lateral intraparietal (LIP) area exhibits visual and saccadic neuronal responses. Electrophysiology, which in essence is a correlation method, cannot entirely solve the question of the functional implication of these areas: are they primarily involved in sensory processing, in motor processing, or in some intermediate function? Lesion approaches (reversible or permanent) in the monkey can provide important information in this respect. Lesions of MT or MST produce deficits in the perception of visual motion, which would argue for their possible role in sensory guidance of ocular pursuit rather than in directing motor commands to the eye muscle. Lesions of LIP do not produce specific visual impairments and cause only subtle saccadic deficits. However, recent results have shown the presence of severe deficits in spatial attention tasks. LIP could thus be implicated in the selection of relevant objects in the visual scene and provide a signal for directing the eyes toward these objects. Functional imaging studies in humans confirm the role of the parietal cortex in pursuit, saccadic, and attentional networks, and show a high degree of overlap with monkey data. Parietal lobe lesions in humans also result in behavioral deficits very similar to those that are observed in the monkey. Altogether, these different sources of data consistently point to the involvement of the parietal cortex in the representation of space, at an intermediate stage between vision and action.     

Behavioral discrimination of water motions caused by moving objects.

We tested whether goldfish, Carassius auratus, discriminate hydrodynamic stimuli caused by moving objects. Blindfolded goldfish responded to a passing object with changes in inter-gill-movement intervals. To learn whether goldfish can discriminate water motions caused by different moving objects we habituated them to a certain object stimulus. If the stimulus was altered, e.g., by altering speed, direction of motion, or size or shape of the object, fish again showed a temporary suspension of breathing when the object passed by. If animals failed to respond to an altered stimulus, we paired this stimulus with a weak electric shock during training. Goldfish discriminated object motion direction. In addition, in two choice experiments goldfish discriminated water motions caused by objects which moved with different speeds (e.g., 5 cm s(-1) versus 6 cm s(-1)), or by objects which differed in size (e.g., 1 cm x 1 cm versus 1.4 cm x 1.4 cm cross section), or shape (e.g., a round versus a triangular object). If object size and/or shape was varied quasi-randomly such that the faster moving object not always caused the greatest water velocities, fish still discriminated object speed.