Binocular coordination of the eyes during reading

Saccadic eye movements and fixations are the behavioral means by which we visually sample text during reading. Human oculomotor control is governed by a complex neurophysiological system involving the brain stem, superior colliculus, and several cortical areas [1, 2]. A very widely held belief among researchers investigating primate vision is that the oculomotor system serves to orient the visual axes of both eyes to fixate the same target point in space. It is argued that such precise positioning of the eyes is necessary to place images on corresponding retinal locations, such that on each fixation a single, nondiplopic, visual representation is perceived [3]. Vision works actively through a continual sampling process involving saccades and fixations [4]. Here we report that during normal reading, the eyes do not always fixate the same letter within a word. We also demonstrate that saccadic targeting is yoked and based on a unified cyclopean percept of a whole word since it is unaffected if different word parts are delivered exclusively to each eye via a dichoptic presentation technique. These two findings together suggest that the visual signal from each eye is fused at a very early stage in the visual pathway, even when the fixation disparity is greater than one character (0.29 deg), and that saccade metrics for each eye are computed on the basis of that fused signal.

The binocular coordination of eye movements during reading in children and adults

Recent evidence indicates that each eye does not always fixate the same letter during reading and there has been some suggestion that processing difficulty may influence binocular coordination. We recorded binocular eye movements from children and adults reading sentences containing a word frequency manipulation. We found disparities of significant magnitude between the two eyes for all participants, with greater disparity magnitudes in children than adults. All participants made fewer crossed than uncrossed fixations. However, children made a higher proportion of crossed fixations than adults. We found no influence of word frequency on children’s fixations and on binocular coordination in adults.

Temporal events in cyclopean vision.

The majority of neurons in the primary visual cortex of primates can be activated by stimulation of either eye; moreover, the monocular receptive fields of such neurons are located in about the same region of visual space. These well-known facts imply that binocular convergence in visual cortex can explain our cyclopean view of the world. To test the adequacy of this assumption, we examined how human subjects integrate binocular events in time. Light flashes presented synchronously to both eyes were compared to flashes presented alternately (asynchronously) to one eye and then the other. Subjects perceived very-low-frequency (2 Hz) asynchronous trains as equivalent to synchronous trains flashed at twice the frequency (the prediction based on binocular convergence). However, at higher frequencies of presentation (4-32 Hz), subjects perceived asynchronous and synchronous trains to be increasingly similar. Indeed, at the flicker-fusion frequency (approximately 50 Hz), the apparent difference between the two conditions was only 2%. We suggest that the explanation of these anomalous findings is that we parse visual input into sequential episodes.

Plaid motion rivalry: Correlates with binocular rivalry and positive mood state

Recently Hupe and Rubin (2003, Vision Research 43 531 - 548) re-introduced the plaid as a form of perceptual rivalry by using two sets of drifting gratings behind a circular aperture to produce quasi-regular perceptual alternations between a coherent moving plaid of diamond-shaped intersections and the two sets of component 'sliding' gratings. We call this phenomenon plaid motion rivalry (PMR), and have compared its temporal dynamics with those of binocular rivalry in a sample of subjects covering a wide range of perceptual alternation rates. In support of the proposal that all rivalries may be mediated by a common switching mechanism, we found a high correlation between alternation rates induced by PMR and binocular rivalry. In keeping with a link discovered between the phase of rivalry and mood, we also found a link between PMR and an individual's mood state that is consistent with suggestions that each opposing phase of rivalry is associated with one or the other hemisphere, with the 'diamonds' phase of PMR linked with the 'positive' left hemisphere.

Binocular interaction:Contrast matching and contrast discrimination are predicted by the same model

How do signals from the 2 eyes combine and interact? Our recent work has challenged earlier schemes in which monocular contrast signals are subject to square-law transduction followed by summation across eyes and binocular gain control. Much more successful was a new 'two-stage' model in which the initial transducer was almost linear and contrast gain control occurred both pre- and post-binocular summation. Here we extend that work by: (i) exploring the two-dimensional stimulus space (defined by left- and right-eye contrasts) more thoroughly, and (ii) performing contrast discrimination and contrast matching tasks for the same stimuli. Twenty-five base-stimuli made from 1 c/deg patches of horizontal grating, were defined by the factorial combination of 5 contrasts for the left eye (0.3-32%) with five contrasts for the right eye (0.3-32%). Other than in contrast, the gratings in the two eyes were identical. In a 2IFC discrimination task, the base-stimuli were masks (pedestals), where the contrast increment was presented to one eye only. In a matching task, the base-stimuli were standards to which observers matched the contrast of either a monocular or binocular test grating. In the model, discrimination depends on the local gradient of the observer's internal contrast-response function, while matching equates the magnitude (rather than gradient) of response to the test and standard. With all model parameters fixed by previous work, the two-stage model successfully predicted both the discrimination and the matching data and was much more successful than linear or quadratic binocular summation models. These results show that performance measures and perception (contrast discrimination and contrast matching) can be understood in the same theoretical framework for binocular contrast vision. © 2007 VSP.

Equivalence of physical and perceived speed in binocular rivalry

The relative dominance of gratings engaged in binocular rivalry can be influenced by their surroundings. One striking example occurs when surrounding motion is congruent with one but not the other grating (C. L. Paffen, S. F. te Pas, R. Kanai, M. J. van der Smagt, & F. A. Verstraten, 2004). However, such center-surround stimulus configurations can also modulate perceived speed, via a directionally tuned process (H. P. Norman, J. F. Norman, J. T. Todd, & D. T. Lindsey, 1996). We recorded rivalry for Gabor patches embedded in a drifting noise texture. Gratings whose directions opposed the background motion tended to dominate more, and vice versa, consistent with previous findings. Observers then matched the speed of a drifting noise-embedded Gabor to that of a Gabor surrounded by mean luminance. Surround motion produced substantial changes in perceived speed, by at least a factor of two for all observers. We then asked whether perceived speed could account for the contextual effects on dominance. We measured the effects of speed on rivalry dominance by changing the physical speeds of rivaling gratings, as determined by the matching data. We found the same pattern of dominance as for the context experiment, indicating that perceived and true speed influence rivalry in the same manner. We propose a Bayesian interpretation of the perceived speed illusion.

On the relation between dichoptic masking and binocular rivalry

When our two eyes view incompatible images, the brain invokes suppressive processes to inhibit one image, and favor the other. Two phenomena are typically observed: dichoptic masking (reduced sensitivity to one image) for brief presentations, and binocular rivalry (alternation between the two images), over longer exposures. However, it is not clear if these two phenomena arise from a common suppressive process. We investigated this by measuring both threshold elevation in simultaneous dichoptic masking and mean percept durations in rivalry, whilst varying relative stimulus orientation. Masking and rivalry showed significant correlations, such that strong masking was associated with long dominance durations. A second experiment suggested that individual differences across both measures are also correlated. These findings are consistent with varying the magnitude of interocular suppression in computational models of both rivalry and masking, and imply the existence of a common suppressive process. Since dichoptic masking has been localised to the monocular neurons of V1, this is a plausible first stage of binocular rivalry.

Suppression and summation in contrast gain control for human vision

Over the last ten years our understanding of early spatial vision has improved enormously. The long-standing model of probability summation amongst multiple independent mechanisms with static output nonlinearities responsible for masking is obsolete. It has been replaced by a much more complex network of additive, suppressive, and facilitatory interactions and nonlinearities across eyes, area, spatial frequency, and orientation that extend well beyond the classical recep-tive field (CRF). A review of a substantial body of psychophysical work performed by ourselves (20 papers), and others, leads us to the following tentative account of the processing path for signal contrast. The first suppression stage is monocular, isotropic, non-adaptable, accelerates with RMS contrast, most potent for low spatial and high temporal frequencies, and extends slightly beyond the CRF. Second and third stages of suppression are difficult to disentangle but are possibly pre- and post-binocular summation, and involve components that are scale invariant, isotropic, anisotropic, chromatic, achromatic, adaptable, interocular, substantially larger than the CRF, and saturated by contrast. The monocular excitatory pathways begin with half-wave rectification, followed by a preliminary stage of half-binocular summation, a square-law transducer, full binocular summation, pooling over phase, cross-mechanism facilitatory interactions, additive noise, linear summation over area, and a slightly uncertain decision-maker. The purpose of each of these interactions is far from clear, but the system benefits from area and binocular summation of weak contrast signals as well as area and ocularity invariances above threshold (a herd of zebras doesn't change its contrast when it increases in number or when you close one eye). One of many remaining challenges is to determine the stage or stages of spatial tuning in the excitatory pathway.

Contrast masking in strabismic amblyopia: attenuation, noise, interocular suppression and binocular summation

To investigate amblyopic contrast vision at threshold and above we performed pedestal-masking (contrastdiscrimination) experiments with a group of eight strabismic amblyopes using horizontal sinusoidal gratings (mainly 3 c/deg) in monocular, binocular and dichoptic configurations balanced across eye (i.e. five conditions). With some exceptions in some observers, the four main results were as follows. (1) For the monocular and dichoptic conditions, sensitivity was less in the amblyopic eye than in the good eye at all mask contrasts. (2) Binocular and monocular dipper functions superimposed in the good eye. (3) Monocular masking functions had a normal dipper shape in the good eye, but facilitation was diminished in the amblyopic eye. (4) A less consistent result was normal facilitation in dichoptic masking when testing the good eye, but a loss of this when testing the amblyopic eye. This pattern of amblyopic results was replicated in a normal observer by placing a neutral density filter in front of one eye. The two-stage model of binocular contrast gain control [Meese, T.S., Georgeson, M.A. & Baker, D.H. (2006). Binocular contrast vision at and above threshold. Journal of Vision 6, 1224--1243.] was `lesioned' in several ways to assess the form of the amblyopic deficit. The most successful model involves attenuation of signal and an increase in noise in the amblyopic eye, and intact stages of interocular suppression and binocular summation. This implies a behavioural influence from monocular noise in the amblyopic visual system as well as in normal observers with an ND filter over one eye.

Binocular contrast interactions:Dichoptic masking is not a single process

To decouple interocular suppression and binocular summation we varied the relative phase of mask and target in a 2IFC contrast-masking paradigm. In Experiment I, dichoptic mask gratings had the same orientation and spatial frequency as the target. For in-phase masking, suppression was strong (a log-log slope of ∼1) and there was weak facilitation at low mask contrasts. Anti-phase masking was weaker (a log-log slope of ∼0.7) and there was no facilitation. A two-stage model of contrast gain control [Meese, T.S., Georgeson, M.A. and Baker, D.H. (2006). Binocular contrast vision at and above threshold. Journal of Vision, 6: 1224-1243] provided a good fit to the in-phase results and fixed its free parameters. It made successful predictions (with no free parameters) for the anti-phase results when (A) interocular suppression was phase-indifferent but (B) binocular summation was phase sensitive. Experiments II and III showed that interocular suppression comprised two components: (i) a tuned effect with an orientation bandwidth of ∼±33° and a spatial frequency bandwidth of >3 octaves, and (ii) an untuned effect that elevated threshold by a factor of between 2 and 4. Operationally, binocular summation was more tightly tuned, having an orientation bandwidth of ∼±8°, and a spatial frequency bandwidth of ∼0.5 octaves. Our results replicate the unusual shapes of the in-phase dichoptic tuning functions reported by Legge [Legge, G.E. (1979). Spatial frequency masking in human vision: Binocular interactions. Journal of the Optical Society of America, 69: 838-847]. These can now be seen as the envelope of the direct effects from interocular suppression and the indirect effect from binocular summation, which contaminates the signal channel with a mask that has been suppressed by the target. © 2007 Elsevier Ltd. All rights reserved.

A reevaluation of achromatic spatio-temporal vision: nonoriented filters are monocular, they adapt, and can be used for decision making at high flicker speeds

Masking, adaptation, and summation paradigms have been used to investigate the characteristics of early spatio-temporal vision. Each has been taken to provide evidence for (i) oriented and (ii) nonoriented spatial-filtering mechanisms. However, subsequent findings suggest that the evidence for nonoriented mechanisms has been misinterpreted: those experiments might have revealed the characteristics of suppression (eg, gain control), not excitation, or merely the isotropic subunits of the oriented detecting mechanisms. To shed light on this, we used all three paradigms to focus on the ‘high-speed’ corner of spatio-temporal vision (low spatial frequency, high temporal frequency), where cross-oriented achromatic effects are greatest. We used flickering Gabor patches as targets and a 2IFC procedure for monocular, binocular, and dichoptic stimulus presentations. To account for our results, we devised a simple model involving an isotropic monocular filter-stage feeding orientation-tuned binocular filters. Both filter stages are adaptable, and their outputs are available to the decision stage following nonlinear contrast transduction. However, the monocular isotropic filters (i) adapt only to high-speed stimuli—consistent with a magnocellular subcortical substrate—and (ii) benefit decision making only for high-speed stimuli (ie, isotropic monocular outputs are available only for high-speed stimuli). According to this model, the visual processes revealed by masking, adaptation, and summation are related but not identical.

Interocular suppression in normal and amblyopic vision:spatio-temporal properties

We measured the properties of interocular suppression in strabismic amblyopes and compared these to dichoptic masking in binocularly normal observers. We used a dichoptic version of the well-established probed-sinewave paradigm that measured sensitivity to a brief target stimulus (one of four letters to be discriminated) in the amblyopic eye at different times relative to a suppression-inducing mask in the fixing eye. This was done using both sinusoidal steady state and transient approaches. The suppression-inducing masks were either modulations of luminance or contrast (full field, just overlaying the target, or just surrounding the target). Our results were interpreted using a descriptive model that included contrast gain control and spatio-temporal filtering prior to excitatory binocular combination. The suppression we measured, other than in magnitude, was not fundamentally different from normal dichoptic masking: lowpass spatio-temporal properties with similar contributions from both surround and overlay suppression.

Blobs versus bars:psychophysical evidence supports two types of orientation response in human color vision

The classic hypothesis of Livingstone and Hubel (1984, 1987) proposed two types of color pathways in primate visual cortex based on recordings from single cells: a segregated, modularpathway that signals color but provides little information about shape or form and a second pathway that signals color differences and so defines forms without the need to specify their colors. A major problem has been to reconcile this neurophysiological hypothesis with the behavioral data. A wealth of psychophysical studies has demonstrated that color vision has orientation-tuned responses and little impairment on form related tasks, but these have not revealed any direct evidence for nonoriented mechanisms. Here we use a psychophysical method of subthreshold summation across orthogonal orientations for isoluminant red-green gratings in monocular and dichoptic viewing conditions to differentiate between nonoriented and orientation-tuned responses to color contrast. We reveal nonoriented color responses at low spatial frequencies (0.25-0.375 c/deg) under monocular conditions changing to orientation-tuned responses at higher spatial frequencies (1.5 c/deg) and under binocular conditions. We suggest that two distinct pathways coexist in color vision at the behavioral level, revealed at different spatial scales: one is isotropic, monocular, and best equipped for the representation of surface color, and the other is orientation-tuned, binocular, and selective for shape and form. This advances our understanding of the organization of the neural pathways involved in human color vision and provides a strong link between neurophysiological and behavioral data. © 2013 ARVO.