Uri Polat

Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments

We measured contrast detection thresholds for a foveal Gabor signal flanked by two high contrast Gabor signals. The spatially localized target and masks enabled investigation of space dependent lateral interactions between foveal and neighboring spatial channels. Our data show a suppressive region extending to a radius of two wavelengths, in which the presence of the masking signals have the effect of increasing target threshold. Beyond this range a much larger facilitatory region (up to a distance of ten wavelengths) is indicated, in which contrast thresholds were found to decrease by up to a factor of two. The interactions between the foveal target and the flanking Gabor signals are spatial-frequency and orientation specific in both regions, but less specific in the suppression region.

Collinear stimuli regulate visual responses depending on cell's contrast threshold

Neurons in the primary visual cortex are selective for the size, orientation and direction of motion of patterns falling within a restricted region of visual space known as the receptive field. The response to stimuli presented within the receptive field can be facilitated or suppressed by other stimuli falling outside the receptive field which, when presented in isolation, fail to activate the cell. Whether this interaction is facilitative,,, or suppressive,,,, depends on the relative orientation of pattern elements inside and outside the receptive field. Here we show that neuronal facilitation preferentially occurs when a near-threshold stimulus inside the receptive field is flanked by higher-contrast, collinear elements located in surrounding regions of visual space. Collinear flanks and orthogonally oriented flanks, however, both act to reduce the response to high-contrast stimuli presented within the receptive field. The observed pattern of facilitation and suppression may be the cellular basis for the observation in humans that the detectability of an oriented pattern is enhanced by collinear flanking elements. Modulation of neuronal responses by stimuli falling outside their receptive fields may thus represent an early neural mechanism for encoding objects and enhancing their perceptual saliency.

The architecture of perceptual spatial interactions

Lateral interactions between spatial filters were explored with a lateral masking paradigm. Contrast sensitivity (two-alternative forced-choice) for a Gabor signal in the presence of two flanking high contrast Gabor signals (masks) was measured. When the target to mask distance was less than 2 target wavelengths the contrast sensitivity decreased up to a factor of two relative to a no mask condition. At larger separations, up to eight wavelengths, an increase in contrast sensitivity occurred. This increase was maximal at separation distances of 2-3 wavelengths, where sensitivity increased by a factor of two. However, the enhancement magnitude and range was dependent on the offset between the Gabor signal orientation and the direction defined by the virtual line connecting the two masks (global orientation). Maximal effects occurred when this offset was zero (100% increase in sensitivity) and 90 deg (50% increase). A 45 deg offset yielded only a small enhancement (20%). The enhancement dependence on spatial arrangement was found to be invariant across different global orientations (meridian). This pattern of interactions may be involved in grouping colinear line segments into smooth curves.

Functional architecture of long-range perceptual interactions

The pattern of lateral interactions in the primary visual cortex, which has emerged from recent studies, conforms to the grouping rules of similarity, proximity, smoothness and closure. The goal of this paper is to understand the perceptual salience of oriented elements that are specifically organized to form a smooth contour. An overview of recent studies, in combination with new experimental results, is presented here to emphasis the idea that visual responses depend on input from both the center and the surround of the classical receptive field (CRF). It is assumed that normal lateral interactions produce a neuronal network that is formed by two antagonistic mechanisms: (i) excitation, that is spatially organized along the optimal orientation (collinear), and is predominant near the contrast threshold of the neuron, and (ii) inhibition, that is less selective and is distributed diffusely around the cells response field. Thus, the inputs from the CRF and the anisotropic surround are summated non-linearly. The specificity of the facilitation and suppression along the collinear direction suggests the existence of second-order elongated collinear filters, which may increase the response similarity between neurons responding to elongated stimulus, thus may enhance the perceptual salience of anisotropic configurations such as contours. This causal connection is particularly evident in amblyopes, where abnormal development of the network results in the abnormal perception of contours.

Neurophysiological Evidence for Contrast Dependent Long-range Facilitation and Suppression in the Human Visual Cortex

Long-range spatial interactions in human visual cortex were explored using a lateral masking paradigm. Visual evoked potentials (VEPs) elicited by a Gabor signal presented in isolation or in the presence of two flanking high-contrast Gabor signals (masks) were measured. Response amplitude and phase were recorded for a vertically oriented test, for horizontal and vertical masks and for combinations of vertical tests and vertical or horizontal masks. The amplitudes and phases of the test alone and mask alone responses were added coherently to predict the amplitude for collinear and orthogonal lateral masking conditions. Additivity failures were taken as evidence for neural interactions. At a target-to-mask distance of 2 deg, VEP amplitude exceeded the linear prediction for test contrasts in the range of 8-16% for the collinear, co-axial target/mask combination. Measured response phase also led predicted response phase over the same range of contrast. The VEP amplitudes were less than the linear prediction in the orthogonal target/mask combination and measured response phase lagged the predicted phase. Significant facilitation occurred with collinear test/mask combinations up to at least 3 deg of separation (nine wavelengths). Co-oriented, but non-collinear test/mask combinations (oblique test and mask, horizontal test and mask) did not produce facilitation. Contrast gain thus appears to be set over considerable distances in a configuration-specific fashion.

Abnormal long-range spatial interactions in amblyopia.

Neural interactions between widely separated stimuli were explored with psychophysical and visual evoked potential (VEP) measures in normal and amblyopic observers. Contrast detection thresholds were measured psychophysically for small foveally viewed Gabor patches presented in isolation and in the presence of similar, but laterally displaced flanks. The amplitude and phase of VEPs elicited by similar targets were also measured. The presence of neural interaction between the target and flank responses was assessed by comparing the unflanked threshold to the flanked threshold in the psychophysical experiments and by comparing the response predicted by the algebraic sum of test and flank responses to that measured when test and flanks were presented simultaneously. In normal observers simultaneous presentation of test and flank targets produces a VEP response that is up to a factor of two larger than the linear prediction (facilitation). Psychophysical threshold is also facilitated by a comparable factor. Facilitation was found mainly for configurations in which local (carrier) and global (patch) orientations resulted in collinearity, independent of global orientation (meridian). Amblyopic observers showed several deviations from the normal pattern. The facilitation for the collinear configurations was either markedly lower than normal or was replaced by inhibition. The normal pattern of spatial interaction may facilitate the grouping of collinear line segments into smooth curves. In contrast, abnormal long-range spatial interactions may underlie the grouping disorders and perceptual distortions found in amblyopia.

Facilitation and suppression of single striate-cell activity by spatially discrete pattern stimuli presented beyond the receptive field

Visual stimulation of a region outside the receptive field of single cells in visual cortex often results in the modulation of their responses. The modulatory effects are thought to be mediated through lateral connections within visual cortex. Research on lateral interactions commonly shows suppression. There has been no systematic study of the optimal conditions for facilitation. Here we have studied the nature of the modulation using a new type of compound stimulus: contrast reversal of pattern stimuli made of three discrete grating patches. The middle patch, optimally fitted to the receptive field in orientation, size, and spatial as well as temporal frequencies, was flanked by two similar patches presented well outside the receptive field. We found that (1) both facilitation and suppression occurred often in the same cells, when orientations of the target and flankers matched the receptive-fields optimal orientation; (2) facilitation with collinear flankers occurred most frequently at target contrasts just above the cells firing threshold and suppression prevailed at high contrasts; (3) facilitative or suppressive modulation was obtained with target-flankers separation of up to 12 deg or more; (4) collinear facilitation was lost when flankers orientation was rotated by 90 deg, while keeping all other parameters the same; and (5) neither the modulation mode nor the proportion of modulated cells was related to the cell types (simple vs. complex cells) and cells laminar locations. Here we have provided physiological evidence for contrast-dependent, collinear facilitation probably underlying perceptual grouping in humans.

A new test of contour integration deficits in patients with a history of disrupted binocular experience during visual development

Previous studies have suggested that the integration of orientation information across space is impaired in amblyopia. We developed a method for quantifying orientation-domain processing using a test format that is suitable for clinical application. The test comprises a graded series of cards where each card includes a closed path (contour) of high contrast Gabor signals embedded in a random background of Gabor signals. Contour visibility in both normals and patients with histories of abnormal binocular vision depends jointly on the spacing of elements on the contour as well as background element density. Strabismic amblyopes show significant degradation of performance compared to normals. Small but significant losses in sensitivity were also observed in a group of non-amblyopic strabismus patients. Threshold measurements made with contrast reducing diffusers indicated that the amblyopic loss is not due to the reduced contrast sensitivity of the amblyopic eye. An abnormal pattern of long-range connectivity between spatial filters or a loss of such connectivity appears to be the primary source of contour integration deficits in amblyopia and strabismus.

What pattern the eye sees best

The visibility of gratings improves with increasing stimulus area. This effect is usually interpreted as being due to physiological summation within the extent of the largest spatial filter and due to probability summation between the outputs of linear, independent filters beyond that range. It is generally assumed that this improvement is isotropic to the patch configuration. In contrast, the existence of long-range facilitation that is configuration-specific suggests that the visibility of a local contrast is dependent on the spatial configuration of the stimuli. We measured contrast thresholds for circular and elongated Gabor patches with a static carrier. The patch envelope orientation was either the same as the bar orientation (collinear) or orthogonal to it. Contrast sensitivity was highest for elongated configurations that were collinear with the grating bars, and reached maximal efficiency at a length of about four grating cycles (eight bar widths), but a width of only one cycle.

Contrast response characteristics of long- range lateral interactions in cat striate cortex

Single-cell responses in visual cortex to a target falling within their receptive field can be modified by collinear flanking stimuli concurrently presented outside the receptive field. Here, we report the presence of four types of contrast-dependent lateral effects: (1) facilitation at low target contrasts and suppression at high contrasts, (2) facilitation that increases with contrast, (3) suppression that increases with contrast, and (4) suppression at low contrasts with facilitation at high contrasts. We propose a sensitivity modulation model that accounts for all the four types of lateral effects by changes in two parameters. In this model, activation of neighboring neurons changes the sensitivities of the target neuron to both the direct feedforward input and inhibitory, divisive feedback from neighboring neurons.