The goal of this study was to see if the persistence of border ownership signals in V2 is an intrinsic property of the figure-ground mechanisms or if it reflects emerging object representations. Considering figure-ground organization as a process in a network of interconnected neurons, it is conceivable that, once the state of the network is set by the input signals, the network remains in that state until new signals arrive at the input that move it into a different state. Thus, if an edge is first assigned to object A, and then a new object B appears and new figure-ground cues indicate that edge should now be assigned to B, the network will switch border ownership to B. In contrast, if the persistence of signals reflects object representations, we expect that an edge that is assigned to one object cannot easily be assigned to another object.
To distinguish between these hypotheses, we created displays in which the figure-ground cues reverse, while the objects remain the same. This was accomplished by displaying two figures, one occluding the other ( left), and then smoothly moving the bottom figure to a new position ( right). The final configuration is typically perceived as a square overlapping a rectangle. The black square that was initially in back now appears in front of the white figure. Thus, after the cessation of movement, the vertical edge in the center changes ownership from left to right. We refer to this condition as CUE REVERSAL (Movie S1
For this test, the cue integration hypothesis predicts that the border ownership signal should change from “left” to “right” as soon as the figure-ground cues reverse. In contrast, the object representation hypothesis predicts persistence of signals, because the representation for the white L shape persists after the cessation of movement.
We tested this display sequence in neurons of area V2. The edge that underwent the change of border ownership was placed in the receptive field of the neuron under study (, red ellipse). For comparison, three other conditions were also tested: One was a similar movement display in which the other figure was in back and moved (). This produced a sequence in which the assignment of the border between the figures does not change (CONSISTENT, Movie S2
). The other two conditions were: presentation of the final overlapping figure configuration without a history (ONSET, , Movie S3
), and a figure-flip condition in which the light figure on the left was deleted while a dark figure appeared on the right (FLIP, , Movie S4
The comparison of the CONSISTENT and CUE REVERSAL conditions is shown in . shows the signals of an example neuron and the population averages. The CONSISTENT display produced a sustained border ownership signal, as expected (blue traces). For the first 500ms, foreground and background are defined by dynamic occlusion as well as geometric cues (shape and T-junctions). After the cessation of movement (time 0), only the geometric cues remain. In both phases the cues indicate ownership-right.
The CUE REVERSAL display is similar, except that the cues in the motion phase indicate ownership-left. Accordingly, the border ownership signal first goes negative (, red traces). After the cessation of movement, the signal remains negative for about 700ms despite the display now being identical to that of the CONSISTENT condition, indicating ownership-right. The two signals slowly approach each other, but do not reach a common level by the end of the fixation period. This shows that the initial border ownership assignment has a long lasting effect despite the presence of new, contradictory figure-ground cues. The results were similar in the two animals (Fig. S1
The variation between individual neurons is illustrated in (see Fig. S2
for the results separated by animal). The signals in CUE REVERSAL were averaged over four time bins, as indicated by double arrows on the time axis. Because the firing rates and hence the amplitudes of the border ownership signals varied widely between neurons, the CUE REVERSAL signal of each neuron was normalized by the mean of its signal in the CONSISTENT condition. The Figure shows that most neurons showed persistence of the negative signal, only slowly approaching the mean CONSISTENT level (represented at 1 in the graph because of the normalization). The median border ownership signals of CUE REVERSAL and CONSISTENT conditions were significantly different in each of the time bins (p<0.05, Wilcoxon signed rank test).
Figure 3 Persistence of the border ownership signals of the individual neurons in the CUE REVERSAL condition. For each neuron, the means of the signal during the four intervals shown by double arrows were calculated and normalized by its mean signal in the CONSISTENT (more ...)
The effect of stimulus history can be seen clearly by comparing the CUE REVERSAL with the ONSET condition (, red and black traces): without history, the signal reaches its maximum value in less than 200ms. Note that for the red and the black curve, visual stimulation is identical after time 0.
In the FLIP condition the border ownership cues reverse, as in CUE REVERSAL, but with the difference that the object of the first assignment is removed at the same time. The result was that the signal reversed quickly (, green trace). Although the signal is first negative, as in CUE REVERSAL, the effect of replacing a figure on one side with a new figure on the opposite side is quite different. Note that the new figure in the FLIP condition is identical to the right figure in CUE REVERSAL at the end of movement. Thus, both conditions stimulated the same receptive fields, producing new edge signals at the same time in the same locations. The critical difference is that the figure to which the edge was initially assigned disappears in FLIP, whereas in CUE REVERSAL it continues to be visible.
Some other differences need to be considered too. (1) ONSET of course included the onset of an edge in the receptive field while this edge was turned on 500ms earlier in the other conditions. The edge onset might explain some of the rapid change. Note, however, that FLIP produced a similar rapid change of the signal at time 0 without an edge transient. (2) The background changed in FLIP, but not in CUE REVERSAL. However the background change is unlikely to have a big influence because other experiments have shown that presentations of figures of the type of the Cornsweet illusion produce border ownership signals very similar to those produced by solid figures (Zhang and von der Heydt, 2010
). In such a “Cornsweet figure”, the color/luminance varies only along a narrow seam at the contours. Thus, border ownership signals depend mainly on responses evoked by the contours. Moreover, we have shown that a change of background color does not interrupt the persistence of signals at an ambiguous edge (O’Herron and von der Heydt, 2009
, ). (3) The reason why FLIP produces a larger signal than CUE REVERSAL is that border ownership signals are larger for isolated figures than for borders between overlapping figures (Qiu et al., 2007
Figure 6 Schematic comparison of the signal dynamics in response to a change of border ownership cues under different conditions. Boxes mark the possible locations of objects in the two display phases, A and B indicate two different objects, and arrows indicate (more ...)
The durations of signal persistence are summarized in . There was a twentyfold difference in persistence between CUE REVERSAL and FLIP: When the owner of the edge disappeared (FLIP condition) the signal changed by 1 Hz in 3 ms, but when it continued to be visible (CUE REVERSAL), the same change took 65 ms. In the ONSET condition, the signal changed equally fast as in the FLIP condition. In the CONSISTENT condition, where occlusion cues continuously pointed in one direction, there was a slow negative signal change, indicating that the signal slowly adapted.
Figure 5 The persistence of border ownership signals in the four conditions illustrated in . Persistence was defined as the inverse of the slope of the signal at the beginning of the final phase, as given by the function fits shown in and (more ...)