The Role of Binocular Disparity in Stereoscopic Images of Objects in the Macaque Anterior Intraparietal Area

Neurons in the macaque Anterior Intraparietal area (AIP) encode depth structure in random-dot stimuli defined by gradients of binocular disparity, but the importance of binocular disparity in real-world objects for AIP neurons is unknown. We investigated the effect of binocular disparity on the responses of AIP neurons to images of real-world objects during passive fixation. We presented stereoscopic images of natural and man-made objects in which the disparity information was congruent or incongruent with disparity gradients present in the real-world objects, and images of the same objects where such gradients were absent. Although more than half of the AIP neurons were significantly affected by binocular disparity, the great majority of AIP neurons remained image selective even in the absence of binocular disparity. AIP neurons tended to prefer stimuli in which the depth information derived from binocular disparity was congruent with the depth information signaled by monocular depth cues, indicating that these monocular depth cues have an influence upon AIP neurons. Finally, in contrast to neurons in the inferior temporal cortex, AIP neurons do not represent images of objects in terms of categories such as animate-inanimate, but utilize representations based upon simple shape features including aspect ratio.     

Fucntional specialization and binocular interaction in the visual areas of rhesus monkey prestriate cortex.

If is is believed that neural mechanisms mediating stereoscopic vision may be localized in specific areas of the visual cortex, then it becomes necessary to be able to define these areas adequately. This is no easy matter in the rhesus monkey, an animal close to man, where the cytoarchitecturally uniform prestriate cortex is folded into deep sulci with secondary gyri. One way around this awkward problem is to use the callosal connections of the prestriate cortex as the anatomical landmarks. Callosal connections are restricted to regions at which the vertical meridian is represented. Since the visual fields, including the vertical meridian, are separately represented in each area, each has its own callosal connections. These are of great help in defining some of the boundaries of these areas, since the boundaries often coincide with the representation of the vertical meridian. With the visual areas thus defined anatomically, it becomes relatively easy to assign recordings to particular areas. Studies of binocular interactions in these areas reveal that most cells in all prestriate areas are binocularly driven. Hence, theoretically, all of the prestriate areas are candidates for stereoscopic mechanisms. The degree of binocular interaction varies from cell to cell. At the two extremes are cells which either respond to monocular stimulation only and are inhibited by binocular stimulation or ones which respond to binocular stimulation only. Changing, as opposed to fixed, disparity is signalled by two types of cells. In one category are cells activated in opposite directions for the two eyes. Such cells are always binocularly driven. In the other category are cells, some of which are monocularly activated, that are capable of responding to changing image size. In the monkey, both these categories of cells have so far been found in the motion area of the superior temporal sulcus only.     

Stereopsis and the random element in the organization of the striate cortex.

Receptive field position and orientation disparities are both properties of binocularly discharged striate neurons. Receptive field position desparities have been used as a key element in the neural theory for binocular depth discrimination. Since most striate cells in the cat are binocular, these position disparities require that cells immediately adjacent to one another in the cortex should show a random scatter in their monocular receptive field positions. Superimposed on the progressive topographical representation of the visual field on the striate cortex there is experimental evidence for a localized monocular receptive field position scatter. The suggestion is examined that the binocular position disparities are built up out of the two monocular position scatters. An examination of receptive field orientation disparities and their relation to the random variation in the monocular preferred orientations of immediately adjacent striate neurons also leads to the conclusion that binocular orientation disparities are a consequence of the two monocular scatters. As for receptive field position, the local scatter in preferred orientation is superimposed on a progressive representation of orientation over larger areas of the cortex. The representation in the striate cortex of visual field position and of stimulus orientation is examined in relation to the correlation between the disparities in receptive field position and preferred orientation. The role of orientation disparities in binocular vision is reviewed.     

Stereoscopic mechanisms: binocular responses of the striate cells of cats to moving light and dark bars

New knowledge concerning the internal structure and response properties of the receptive fields of striate cells calls for a fresh appraisal of their binocular interactions in the interest of a better understanding of the neural mechanisms underlying binocular depth discrimination. Binocular position-disparity response profiles were recorded from 71 simple and B-cells in response to moving light and dark bars. Predominantly excitatory (PE) cells (N = 48) had disparity response profiles that were spatially closely similar to their respective monocular responses. In addition, the centrally located excitatory subregions were flanked on one or both sides by non-specific inhibitory regions. PE cells with a preferred stimulus orientation within 30 degrees of the vertical (N = 17) showed binocular facilitations with maximal values that were always more than twice (mean 3.3) the sum of the two monocular responses to the same stimuli and generally greater than the facilitations shown by cells with orientations more than 30 degrees from the vertical (N = 29; mean 2.2 times the sum of the respective monocular responses). The strength of the binocular facilitation depended on the stimulus contrast, the facilitation decreasing with increasing contrast. The receptive-field disparity distribution of the 31 PE cells capable of making significant horizontal disparity discriminations has standard deviations of 0.37 degrees and 0.40 degrees, respectively. Predominantly inhibitory cells (PI) (N = 23) showed two basic types of disparity response profile: symmetric (N = 17) and asymmetric (N = 6). Uncertainty regarding the precise location of the binocular fixation point in the anaesthetized and paralysed preparation made it difficult to categorize PI cells adequately.     

The effect of binocular stimulation on each component of transient and steady-state VEPs

We recorded the monocular and binocular VEPs to the alternation of sinusoidal gratings in order to evaluate the binocular interaction in each component of transient and steady-state VEPs in 13 normal subjects. Three spatial frequencies (1.3, 2.6 and 5.3 c/deg) with a 90% contrast were used as visual stimuli. The latencies and amplitudes of N70 and P100 of the transient VEPs were measured. The steady-state VEPs were Fourier analyzed, and both the phase and amplitude of the second (2F) and fourth (4F) harmonic responses were obtained. Binocular interaction was influenced by spatial frequency such that a binocular summation or even an inhibition occurred. For the transient VEPs, a binocular summation was more pronounced in the amplitude of N70 than in that of P100 at all spatial frequencies. There were no significant effects of binocular stimulation on latencies of N70 or P100. However, the latencies of N70 and P100 showed different spatial frequency characteristics. For the steady-state VEPs, the amplitude of 2F revealed a binocular summation that was more pronounced at 5.3 c/deg, whereas the 4F amplitude showed binocular inhibition at 2.6 and 5.3 c/deg. The 2F phase showed binocular inhibition at all spatial frequencies, whereas no such inhibition was observed in the 4F phase. These results suggest that individual components of transient and steady-state VEPs are physiologically distinct and may therefore be generated from different neuronal populations in striate cortex.     

Stereoscopic correspondence for ambiguous targets is affected by elevation and fixation distance

Binocular correspondence must be determined if disparity is to be used to provide information about three-dimensional shape. The current study investigated whether knowledge of the statistical distribution of disparities in the natural environment is employed in this process. A simple model, which produces distributions of distances similar to those found in the natural environment, was used to predict the distribution of disparities in natural images. This model predicts that crossed disparities will be more likely as (i) stimulus elevation decreases below fixation and (ii) fixation distance increases. To determine whether these factors influence binocular correspondence for human observers, ambiguous stereograms were presented to observers, as stimulus elevation and fixation distance were manipulated. Clear biases were observed in the depth perceived in these stereograms, which were more likely to be seen as closer than fixation (i) for stimuli presented below fixation and (ii) as fixation distance increased. These results suggest that binocular correspondence is determined in a manner consistent with the distributions of disparities expected in natural scenes.     

Hemispheric specialization for global and local processing: the effect of stimulus category.

Neuropsychological evidence indicates that the global aspect of complex visual scenes is preferentially processed by the right hemisphere, and local aspects are preferentially processed by the left hemisphere. Using letter-based hierarchical stimuli (Navon figures), we recently demonstrated, in a directed-attention task, lateralized neural activity (assessed by positron emission tomography) in the left prestriate cortex during local processing, and in the right prestriate cortex during global processing. Furthermore, temporal-parietal cortex was critically activated bilaterally in a divided-attention task that involved varying the number of target switches between local and global levels of letter-based hierarchical stimuli. Little is known about whether such stimulus categories influence such hemispheric lateralization. We now present data on brain activity, derived from positron emission tomography, in normal subjects scanned during either local or global processing of object-based hierarchical stimuli. We again observe attentional modulation of neural activity in prestriate cortex. There is now greater right-sided activation for local processing and greater left-sided activation for global processing, which is the opposite of that seen with letter-based stimuli. The results suggest that the relative differential hemispheric activations in the prestriate areas during global and local processing are modified by stimulus category.     

Effect of fast moving stimuli and saccadic eye movements on cell activity in visual areas V1 and V2 of behaving monkeys

Extracellular recordings were carried out in the visual cortex of behaving monkeys trained on a fixation/detection task, during which a target light was displayed stationary or suddenly moving on a tangent translucent screen. The responses of visual cortical cells to fast moving stimuli during steady fixation and those obtained during rapid eye movements (saccades) which moved their receptive field across a stationary stimulus, were studied. Areas V1 and V2 were explored. When tested with rapidly moving stimuli (500 deg/sec) during steady fixation, neurons in each area behaved in almost the same way. About one fourth of them were activated, the remainder showing either no response (little more than a half of them) or a reduction of the spontaneous firing rate. In both areas, some of the neurons activated during steady fixation did not respond or responded very weakly during eye motion at saccadic velocity (500 +/- 50 deg/sec). Neurons of this type, which we refer to as 'real motion' cells, could somehow contribute to the maintenance of visual stability during the execution of large eye movements.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

A spatial property of the retino-cortical mapping

Striate cortex topography derives from a stretching of retinal space along the optic axis. At the retina, relative distances are preserved in a mapping of retinal space onto a spherical surface in the environment. At the cortex, relative distances along visual meridia in the cortical map are preserved in a mapping of striate cortex onto an environmental conic surface whose base is in the plane of the eye. This eco-cortical relationship can be considered a reference frame through which spatial relationships at the cortex might provide information about the environment. The present analysis provides an explanation of changes in cortical magnification with visual eccentricity in the primate and a detailed three-dimensional model of striate topography for the macaque monkey. In man, a conic environmental surface is shown to be uniformly resolvable along meridia in the visual field. Finally, the implications of this analysis of the structural properties of the retino-striate pathway and visual resolution are considered in relation to depth and distance perception.     

Stereoscopic vision: what's the first step?

Neurons in primary visual cortex respond to binocular disparity, the raw material of stereoscopic depth perception. Although these neurons are probably essential to depth perception, a recent study has shown that they are unable to compute depth itself.     

Dyslexic children are confronted with unstable binocular fixation while reading

Reading requires three-dimensional motor control: saccades bring the eyes from left to right, fixating word after word; and oblique saccades bring the eyes to the next line of the text. The angle of vergence of the two optic axes should be adjusted to the depth of the book or screen and--most importantly--should be maintained in a sustained manner during saccades and fixations. Maintenance of vergence is important as it is a prerequisite for a single clear image of each word to be projected onto the fovea of the eyes. Deficits in the binocular control of saccades and of vergence in dyslexics have been reported previously but only for tasks using single targets. This study examines saccades and vergence control during real text reading. Thirteen dyslexic and seven non-dyslexic children read the French text "L'Allouette" in two viewing distances (40 cm vs. 100 cm), while binocular eye movements were measured with the Chronos Eye-tracking system. We found that the binocular yoking of reading saccades was poor in dyslexic children (relative to non-dyslexics) resulting in vergence errors; their disconjugate drift during fixations was not correlated with the disconjugacy during their saccades, causing considerable variability of vergence angle from fixation to fixation. Due to such poor oculomotor adjustments during reading, the overall fixation disparity was larger for dyslexic children, putting larger demand on their sensory fusion processes. Moreover, for dyslexics the standard deviation of fixation disparity was larger particularly when reading at near distance. We conclude that besides documented phoneme processing disorders, visual/ocular motor imperfections may exist in dyslexics that lead to fixation instability and thus, to instability of the letters or words during reading; such instability may perturb fusional processes and might--in part--complicate letter/word identification.     

Stereoscopic vision: solving the correspondence problem

Neurons in early visual areas respond to horizontal disparity in images that do not give rise to stereopsis. False binocular matches, however, are discarded at the apex of the visual pathway: the activity of neurons in the primate inferior temporal cortex correlates directly with conscious depth perception.     

Mouse visual cortex

Neurons in mouse visual cortex have diverse receptive field properties and they respond selectively to specific features of visual stimuli. Owing to the lateral position of the eyes, only about a third of the visual cortex receives input from both eyes, but many cells in this region are binocular. Similar to higher mammals, closing one eye during a critical period shifts the responses of cells, such that they are better driven by the non-deprived eye. In this review I illustrate how the combination of transgenic mouse technology with single cell recording and modern imaging techniques might lead to a further understanding of the mechanisms that underlie the development, plasticity, and function of the mammalian visual cortex.     

Prey orienting in frogs: Accounting for variations in output with stimulus distance

Summary We have studied the responses of leopard frogs,Rana pipiens, to live mealworms presented at different distances on the mid-sagittal plane. The response of normal frogs to stimuli at nearer distances consists of a direct snap whose amplitude increases with stimulus distance. For greater distances, the response consists of a forward hop whose amplitude also varies with stimulus distance. Over an intermediate range of distances, responses may be either snaps or hops. Whichever response occurs is of appropriate amplitude. The distance at which frogs switch from predominantly snapping responses to predominantly hopping responses increases with body size.Like normal frogs, unilaterally blinded frogs respond to stimuli at nearer distances with snaps whose amplitude varies with stimulus distance, switch from snapping to hopping over an intermediate range of distances, and respond to stimuli at greater distances with hops whose amplitude also increases with stimulus distance. In many cases, unilateral blinding did however result in a decrease in the distance at which the frogs switched from snapping to hopping. Such changes were not accompanied by the changes in snap or hop amplitude which would be expected if unilateral blinding resulted in generalized changes in distance judgement. Normal variations in snap amplitude and switches from snapping to hopping were also observed in frogs subjected to unilateral eye removal prior to the metamorphic eye migration which creates the adult binocular visual field.These results imply that neither distance discrimination nor any of the kinds of variation in motor output which occur with increasing stimulus distance necessarily depend on binocular cues. The behaviors studied also appear to be largely independent of normal binocular experience. More generally, our results suggest that the movement triggered by a stimulus at a particular location is not determined entirely by the retinal and superficial tectal region activated but rather reflects a combination of a retinal local sign signal with other kinds of information. The latter probably include signals related to stimulus distance and body posture, and may include signals related to body size as well.     

Fix your eyes in the space you could reach: neurons in the macaque medial parietal cortex prefer gaze positions in peripersonal space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping.     

Neuromagnetic evidence that the P100 component of the pattern reversal visual evoked response originates in the bottom of the calcarine fissure

Visual evoked magnetic fields due to pattern reversal stimuli were measured in 5 normal subjects using a helmet-shaped 66 channel magnetoencephalography system linked to MRI. The magnetic topography of the prominent 100 ms response (P100m) evoked by full-field visual showed a double-dipole pattern in the occipital areas of all subjects. Right or left half-field stimuli and upper or lower quadrant-field stimuli evoked a single-dipole pattern in the contralateral occipital area. The P100m sources were when localized using a current dipole model and superimposed on MRI images of each subject. The visual cortex was morphologically variable among the subjects, but the P100m dipoles were all localized at the lateral bottom of the calcarine fissure. Moreover, these P100m dipoles had similar orientations for both half- or quadrant-field stimuli. These results suggest that the P100m is located in a smaller part of the striate cortex than previously reported.     

Depth resolution in the pigeon

Summary Pigeons possess a binocular visual field and a retinal region of higher cellular density pointing to the center of this overlap. These features and the precision of pecking behavior suggest that in this lateral-eyed bird cues other than monocular ones might participate in depth judgements.Pigeons were trained with an operant procedure to discriminate between luminous points differing in depth which appeared to the observer as floating in the dark. The accuracy of depth judgements was found to be a function of the ratio between the interstimulus distance and the mean eyes-to-stimulus distance. In a first test (experiment I) no external binocular disparity cues were available, the animal only seeing one luminous point at a time (near or far). In a second test (experiment II) where binocular disparity cues were available, the animal having this time to discriminate a pair of points placed at equal depth from a pair placed at unequal depths, only one pair being visible at a time, depth resolution did not improve. This suggests that, at least within the range of distances explored, the pigeon has no stereoscopic vision. Notwithstanding this, binocular cues do play a role, since when tests were done comparing binocular with monocular viewing (experiment III), monocular depth resolution was significantly worse.     

Evidence for surface-based processing of binocular disparity

It is convenient to think of an object's location as a point within a Cartesian framework; the x axis corresponds to right and left, the y axis to up and down, and the z axis to forward or backward. When an observer is looking straight ahead, binocular disparities provide information about distance along the z axis from the fixation plane. In this coordinate system, changes in disparity are treated as independent of changes in location along the orthogonal x and y axes. Does the human visual system use this three-dimensional coordinate system, or does it specify feature location in a coordinate frame determined by other nearby visible features? Here we show that the sensitivity of the human stereo system is determined by the distance of points with respect to a local reference plane, rather than by the distance along the z axis with respect to the fixation plane. There is a distinct advantage to using a local frame of reference for specifying location. It obviates the need to construct a complex three-dimensional space in either eye-centered or head-centered coordinates that must be updated with every shift of the eyes and head.     

Binocular visual processing in the owl's telencephalon.

Single neurons recorded from the owl's visual Wulst are surprisingly similar to those found in mammalian striate cortex. The receptive fields of Wulst neurons are elaborated, in an apparently hierarchical fashion, from those of their monocular, concentrically organized inputs to produce binocular interneurons with increasingly sophisticated requirements for stimulus orientation, movement and binocular disparity. Output neurons located in the superficial laminae of the Wulst are the most sophisticated of all, with absolute requirements for a combination of stimuli, which include binocular presentation at a particular horizontal binocular disparity, and with no response unless all of the stimulus conditions are satisfied simultaneously. Such neurons have the properties required for 'global stereopsis', including a receptive field size many times larger than their optimal stimulus, which is more closely matched to the receptive fields of the simpler, disparity-selective interneurons. These marked similarities in functional organization between the avian and mammalian systems exist in spite of a number of structural differences which reflect their separate evoluntionary origins. Discussion therefore includes the possibility that there may exist for nervous systems only a very small number of possible solutions, perhaps a unique one, to the problem of stereopsis.