Center-surround antagonism based on disparity in primate area MT

Abstract

Most neurons in primate visual area MT have a large, modulatory region surrounding their classically defined receptive field, or center. The velocity tuning of this "surround" is generally antagonistic to the center, making it potentially useful for detecting image discontinuities on the basis of differential motion. Because classical MT receptive fields are also disparity-selective, one might expect to find disparity-based surround antagonism as well; this would provide additional information about image discontinuities. However, the effects of disparity in the MT surround have not been studied previously. We measured single-neuron responses to variable-disparity moving patterns in the MT surround while holding a central moving pattern at a fixed disparity. Of the 130 neurons tested, 84% exhibited a modulatory surround, and in 52% of these, responses were significantly affected by disparity in the surround. In most cases, disparity effects in the surround were antagonistic to the center; that is, neurons were generally suppressed when center and surround stimuli had the same disparity, with decreasing suppression as the center and surround stimuli became separated in depth. Also, the effects of disparity and direction were mainly additive; i.e., disparity effects were generally independent of direction, and vice versa. These results suggest that the MT center-surround apparatus provides information about image discontinuities, not only on the basis of velocity differences but on the basis of depth differences as well. This supports the hypothesis that MT surrounds have a role in image segmentation.

Fig. 1.

Disparity effects in the MT surround were measured by placing a moving random dot pattern in the receptive field center and three moving patterns in the surround. The central pattern was always the same, moving in the preferred direction and at the preferred disparity (as defined for the center). The opposing arrowsin the surround patterns are meant to indicate that these patterns moved either in the same direction as the center, or in the opposite direction, on different trials (but not simultaneously in both directions). Also, surround patterns were shown at different disparities on different trials. All three surround patterns were identical to each other; i.e., on a given trial they moved in the same direction and had the same disparity (so they appeared to be in the same depth plane).

Fig. 2.

Disparity effects in the classical MT receptive field. The left panel shows an example of disparity tuning in an MT neuron. The points and error bars are means ± SE. The firing rate was strong at negative (near) disparities, and in this example, nil at positive (far) disparities. The right panelshows the distribution of preferred disparities for the entire neuron sample (n = 127). Neurons were classified as near-tuned, far-tuned, or fixation-tuned, depending on the disparity at which the peak response occurred (see Results). The distribution shows that near-tuned cells were more common than fixation-tuned or far-tuned cells.

Fig. 3.

Disparity effects in the receptive field surround. The left panel shows an example based on a single MT neuron. Points and error bars are means ± SE. The two tuning curves were generated while holding a central pattern at a fixed disparity (the preferred disparity for the center). Closed circles show data for surround patterns moving in the same direction as the center pattern; open circles indicate opposite-direction surrounds. For both directions, firing rates increase as surround disparities go from negative to positive (near to far). However, firing rates were higher overall for opposite-direction surrounds, as was typically the case. The right panels show the distribution of preferred disparities in the surround. For both same- and opposite-direction surrounds, the cells tend to prefer far disparities.

Fig. 4.

Examples of the different cell types, as classified by two-way ANOVA. Each panel shows data from a representative cell. In all panels, points and error bars represent means ± SE, and the dashed horizontal line represents the mean response to the central pattern by itself. Closed circles represent surround patterns moving in the same direction as the central pattern; open circles represent opposite-direction surrounds. Baseline firing rates were notsubtracted before graphing the data. A, An additive effect, where direction and disparity both influence the firing rate, but each effect is largely independent of the other. B, Only a direction effect. The opposite-direction surrounds produce a higher response than same-direction surrounds, but there is no appreciable effect of disparity; i.e., the curves are flat. C, Only a disparity effect. For both surround directions, responses increase as disparities go from negative to positive, but there is no significant offset between curves representing same- and opposite-direction surrounds. D, An interactive effect. Both direction and disparity affect the firing rate, but the magnitude of the direction effect depends on disparity and vice versa. E, A nonspecific effect. Responses are suppressed, overall, compared with the response to the central pattern by itself (dashed horizontal line), but responses are roughly constant for different directions and disparities. F, No effect. All responses, regardless of direction or disparity, are roughly equal to the response to the central pattern by itself.

Fig. 5.

Schematic showing how two-way ANOVA tries to explain responses by adding the effects of direction and disparity. Each curve represents the disparity tuning profile for a given direction (same or opposite with respect to the central pattern). The disparity effect is seen as the range of responses going from the base to the peak of a given tuning curve, and the direction effect is seen as the vertical offset between the curves. In this example, it is assumed that there is no interaction; i.e., the two curves are parallel. In the absence of an interaction, the total effect is simply the sum of the direction and disparity effects.

Fig. 6.

Schematic showing how direction effects could reverse at different disparities (top), and how disparity effects could reverse for different directions (bottom). For a disparity reversal, we would see increases in one curve associated with decreases in the other curve and vice versa. For a direction reversal, the order of responses corresponding to the two surround directions would be opposite at different disparities.

Fig. 7.

Example of specific suppressive and excitatory effects in a given neuron. Points and error bars represent mean responses ± SE, and the dashed horizontal linerepresents the mean response to the central pattern by itself. Eachasterisk represents a significant difference (p < 0.05, t test) between the response in question and the response to the central pattern alone. For same-direction surrounds (solid circles), all nine responses were significantly suppressed. For opposite-direction surrounds, three of the nine responses were significantly facilitated.

Fig. 8.

Schematic illustrating how regression can be used to compare the shapes of disparity tuning curves. A andB represent disparity tuning curves under two different conditions. C plots the responses from B(ordinate) against the responses from A (abscissa). Because the curves in A and B have vertically opposite (inverted) shapes, the slope in C is negative. If instead their shapes were similar, the slope in C would be positive.x is disparity, Y is the response to a given disparity in the center, and Z is the response to a given disparity in the surround. Because Y =f(x) (A) and Z= f(x) (B) were measured at the same x values (disparities), Z =f(Y), the relationship between center and surround tuning (C) is known for the measured set of x values.

Fig. 9.

Relationship between disparity tuning in the center and the surround. All panels, open and closed circles represent opposite- and same-direction surrounds (relative to center). A–C, Data from a neuron with opposite disparity tuning in the center and surround. A, Disparity tuning for the center of the receptive field. B, Disparity tuning in the surround, while holding the central pattern at a constant disparity. A, B, Points and error bars are mean responses ± SE. C, Regression of responses to surround disparities versus responses to center disparities (see Fig. 8). Slopes were calculated separately for same- and opposite-direction surrounds. The negative slope in both cases implies that vertical trends were opposite in the center versus the surround. D–F are analogous to A–C but show data from a different neuron in which disparity tuning was similar in the center and the surround (thus positive slopes in F).

Fig. 10.

Pooled data from “additive” cells (n = 30). The dashed horizontal linerepresents the response to the central pattern by itself (normalized to be 100%). Each bar shows mean normalized response, ± SE, for various combinations of direction and disparity. Responses were typically lowest (left bar) when center and surround patterns had different directions and disparities and highest (right bar) when both direction and disparity were different. The middle bars show that a difference in direction or disparity was sufficient to restore firing to the unsuppressed rate (i.e., not different from 100% of the center-alone response).

Fig. 11.

Hypothetical situation showing why surrounds must be antagonistic to the center in terms of direction, speed,and disparity to reliably detect object movement relative to background. An observer is assumed to be moving along a straight path while tracking a stationary object off to the left. This causes the background to move right across the retina. An object moving relative to background will always create a differential velocity on the retina, provided it is close to the background (top panels). If the object moves left with substantial speed (top panel), its retinal motion will be opposite in direction to the background motion. If it is moving right (middle panel), it will move in the same direction as the background but at a higher speed. However, if the object is in the foreground and moving right, its retinal velocity may match the retinal velocity of the background. In this case, its disparity must be different from the background, and this provides a center–surround differential with respect to depth. Because center–surround interactions in MT are direction-, speed-, and disparity-antagonistic, any of these three conditions is sufficient to “unsuppress” neurons with receptive fields centered on the moving object. In contrast, neurons that see background motion in both the center and the surround should remain suppressed.