Alan W. Freeman

Increasing depth of binocular rivalry suppression along two visual pathways.

Binocular rivalry refers to the alternating perception that occurs when the two eyes are presented with incompatible stimuli: one monocular image is seen exclusively for several seconds before disappearing as the other image comes into view. The unseen stimulus is physically present but is not perceived because the sensory signals it elicits are suppressed. The neural site of this binocular rivalry suppression is a source of continuing controversy. We psychophysically tested human subjects, using test probes designed to selectively activate the visual system at a variety of processing stages. The results, which apply to both form and motion judgements, show that the sensitivity loss during suppression increases as the subjects task becomes more sophisticated. We conclude that binocular rivalry suppression is present at a number of stages along two visual cortical pathways, and that suppression deepens as the visual signal progresses along these pathways.

The depth and selectivity of suppression in binocular rivalry

Binocular rivalry occurs when the two eyes are presented with incompatible stimuli and the perceived image alternates between the two stimuli. The aim of this study was to find out whether the periodic perceptual loss of a monocular stimulus during binocular rivalry is mirrored by a comparable loss of contrast sensitivity. We presented brief test stimuli to one eye while its conditioning stimulus was dominant or suppressed. The test stimuli were varied widely across four stimulus domains—namely, the relative stimulation of medium- and long-wavelength-sensitive cones, duration, spatial frequency, and grating orientation. The result in each case was the same. Suppression depended slightly or not at all on the type of test stimulus, and contrast sensitivity during suppression was around 64% of that during dominance. The effect of suppression on sensitivity is therefore very weak, relative to its effect on the perceived image. Furthermore, suppression was largely independent of the similarity between the conditioning and the test stimuli, indicating that our results are better explained byeye suppression than bystimulus suppression. A model is presented to account for the small, monocular sensitivity loss during suppression: It assumes that test detection precedes conditioning stimulus perception in the visual pathway.

Visual loss during interocular suppression in normal and strabismic subjects

Visual acuity was measured in one eye during monocular vision, and while the fellow eye viewed stimuli not including the acuity target. The aim was to find how acuity in one eye is reduced by going from monocular to binocular viewing. In normal subjects, acuity was at its lowest during the suppressive phase of binocular rivalry, was reduced less when the fellow eye viewed a contoured nonrivalrous stimulus, and was not reduced at all when the stimulus to the fellow eye consisted of a uniformly lit field. In strabismic subjects, by contrast, acuity was markedly reduced in going from monocular to binocular viewing no matter what stimulus was viewed by the fellow eye. Pathological suppression is therefore largely independent of the inducing stimulus. It was also shown that acuity in the nonstrabismic eye of some of the strabismic subjects was improved by allowing the strabismic eye to view; these were the subjects with the greatest depths of amblyopia.

Cross-orientation interactions in human vision

Humans can discriminate one visual contour from another on the basis of small differences in orientation. This capability depends on cortical detectors that are selective for a small range of orientations. We have measured this orientation bandwidth and the suppression that helps to shape it, with a reverse correlation technique. Human subjects were presented with a stream of randomly oriented gratings at a rate of 30 per second. Their task was to press a key whenever they saw an orientation nominated as the target. We analyzed the data by finding the probability density of two orientations: One preceded the key-press by the reaction time, and the second preceded the first by up to 100 ms. The results were as follows: (1) One grating facilitated the following one in producing a key-press when the gratings differed little in orientation. The estimate of orientation bandwidth resulting from this facilitation was 38 degrees . (2) A large angle between the two orientations reduced the probability of a key-press. This finding was best modelled as a suppression that did not vary with orientation, consistent with the idea that cross-orientation suppression is non-oriented. (3) Analysis of non-consecutive grating pairs showed that cross-orientation interactions lasted no longer than 67 ms.

Measuring perception without introspection

Binocular rivalry, the perceptual alternation between incompatible monocular stimuli, is conventionally measured by asking the subject which percept is currently visible. This is problematic because the response is unverifiable, open to response bias, and falsely assumes that the perceptual experience is binary. We overcame these limitations in a new approach that does not require subjective reporting of perceptual state. A brief test stimulus was added to one eyes inducing stimulus at random times and contrasts. The test was presented at one of two spatial locations, the subject indicated which alternative had been shown, and the correctness of the response was recorded as a function of test contrast. Given the random timing of the test stimulus, it was sometimes delivered when the tested eye was dominant and, at other times, suppressed. Accordingly, the psychometric function recorded during rivalry should be a mixture of the dominance and suppression forms of the function. This was indeed the case: The probability of a correct response during rivalry was significantly less than that obtained with a binocularly congruent stimulus. The psychometric function during rivalry was well modeled as a weighted sum of the congruence curve with an assumed suppression curve. Optimal fitting provided estimates of both suppression depth and percept predominance that corresponded closely with estimates obtained with the conventional method. We have therefore characterized rivalry without the uncertainties introduced by the subjects perceptual report. This provides a model that may be applicable to the broader field of perceptual ambiguity.

The rod-cone shift and its effect on ganglion cells in the cat's retina

We examined how several characteristics of cat retinal ganglion cells--receptive field size, spatial resolution, and centre-surround antagonism--change with background illumination. Spectral sensitivity was also measured to see how these changes depend on the rod-cone shift. The radius of the centre mechanism changed very little across the mesopic range. The absence of a change can be attributed to the connections rods make with cones, and to the small spatial spread of rods which connect to a cone. The highest spatial frequency to which a cell could respond dropped sharply with falling background illumination. This loss of spatial resolution is due partly to increasing receptive field size, and partly to loss of contrast gain. Centre-surround antagonism approached zero as background illumination fell. The loss of antagonism could have been due to either a change in the subtractive relationship between centre and surround, or due to a loss of surround strength relative to centre strength; the latter was shown to be the case.

Components of visual acuity loss in strabismus

Strabismus, the misalignment of the visual axis of one eye relative to that of the other eye, reduces visual acuity in the affected eye. Several processes contributing to that loss are: amblyopia, which results in a chronic acuity loss whether or not the fellow eye is viewing; strabismic deviation, which shifts the image of an acuity target onto more peripheral, and therefore less acute, retina when the fellow eye fixates; interocular suppression and binocular masking, which reduce visibility in the strabismic eye due to neural influences from the other eye. We measured the losses due to these processes in nine small-angle strabismic subjects. Amblyopia reduced acuity by a median of 34% relative to its value in subjects with normal binocular vision, and strabismic deviation produced a loss of 44%. Suppression and masking together reduced acuity by 20%, and therefore had substantially less effect than the other factors.

Lengthy suppression from similar stimuli during rapid serial visual presentation

The stimulus at any point in the visual field is rarely static during normal viewing: observer and object movement conspire to produce a continually changing series of stimuli. Our aim was to study both the short- and long-term interactions between responses to a series of stimuli presented at a single visual location. We used rapid serial visual presentation (RSVP) in which the stimuli were randomly oriented gratings delivered at the rate of 30 per second. Human subjects pressed a key whenever they saw a target orientation, for example horizontal. The results were analyzed by finding two orientations before each key-press. The first preceded the key-press by the reaction time, and the second preceded the first by an interval of variable duration. There were two main findings. First, the subject was more likely to press the key when the target was immediately preceded by a grating of similar orientation. This facilitation presumably results from the summation of sub-threshold inputs. Second, a key-press was reduced in probability when a target orientation was preceded by a similar orientation with an interstimulus interval of 100-400 ms. The time course of this suppression is similar to that seen in attentional blink experiments.

SPATIAL CHARACTERISTICS OF THE CONTRAST GAIN CONTROL IN THE CAT'S RETINA

Impulse rate was recorded from X- and Y-type ganglion cells in the cats retina. The stimuli were stationary gratings for which luminance varied sinusoidally with distance across the stimulus, and amplitude varied sinusoidally in time. Y cell fundamental and second harmonic responses recorded at medium to high spatial frequencies advanced in phase with increasing contrast, an effect attributable to the contrast gain control. As spatial frequency increased to the highest value capable of evoking a second harmonic response, the phase of this response became retarded, indicating that the contrast gain control was losing its effect. This result showed that the spatial resolution of the contrast gain control is very close to that of the Y cells rectifying subunits. The observations strongly suggest that the contrast gain control has its effect early in retinal image processing.

A multi-stage model for fundamental functional properties in primary visual cortex.

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (∼4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.