Ординатура / Офтальмология / Английские материалы / Eye Movements A Window on Mind and Brain_Van Gompel_2007

Abstract

Objects found at the end of a saccade serve as spatial landmarks. Here we investigate the landmark-based relocalisation process in four experiments by varying the spatial characteristics of the landmark object. The results of the first experiment show that the efficiency of a landmark is independent of transsaccadic displacements of the landmark object over a wide range of displacements. In an ambiguous mapping of the preand postsaccadic information, the visual system uses the centre of gravity of a stimulus configuration for postsaccadic localisation (Experiment 2 and 3). The final experiment demonstrates that the relational spatial information of the presaccadic layout of target and distractors is considered in the relocalisation process after the saccade. The results suggest that the mapping of preand postsaccadic information is based on spatially crude, low spatial frequency information.

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Because of the anatomy of the human retina and the neural processing in later stages of the visual system, only a small part of the visual scene impinging on the retina can be seen with high resolution. In order to circumvent this shortcoming, humans shift their gaze about every 300 ms, with saccadic eye movements, to the new object of interest. These reorienting saccades are so habitual and automatic, that we are often not even aware of the continuous eye-movement activity. The failure to note the effects of eye movements is quite surprising, however, given the dramatic changes of the retinal visual information each saccade induces. Due to the high angular velocity of the eyes during the saccades there occurs a smearing of the retinal image during the saccade. Moreover, due to the continuously changing orientation of the eyes, the visual system has the task to re-map the changing retinal input into a consistent and stable perceptual frame and into an egocentric representation, which is needed for goal-directed action. In the work presented here we study the role of continuously present information on this relocalisation process, across saccadic eye movements.

Various studies have provided evidence for a suppression of perceptual processing during saccadic eye movements. More specifically, it has been demonstrated that saccadic suppression is most pronounced in the magnocellular pathways of the visual system, that is the pathway that is also responsible for the processing of motion signals (e.g., Burr, Morrone, & Ross, 1994; Ross, Morrone, Goldberg, & Burr, 2001). Recent fMRI studies support this finding. So, Kleiser, Seitz, and Krekelberg (2004) found evidence for a reduction of BOLD-signals immediately before saccade onset in brain areas that receive magnocellular input. This implies that saccade-induced motion signals are suppressed by a specific, saccade-related mechanism.

A consequence of the reduction of motion signals during saccades is that exogenous retinal movements due to motion of an object in the world are also prevented from being processed and registered. While detection of a small motion during fixation may be perfect, the sensitivity to movements during saccades is reduced by about four log units (Macknik, Fisher, & Bridgeman, 1991). In a classical paper, Bridgeman, Hendry, and Stark (1975) showed that an object displacement of up to about 30% of the saccade size goes unnoticed, provided that the displacement occurs during or close to the saccade. This finding is in contrast to theories that assume a cancellation of the retinal motion by extraretinal signals for perception (e.g., von Holst & Mittelstaedt, 1950; Sperry, 1950); without further assumptions these theories would predict that even a small transsaccadic displacement should be perceivable. This has lead some authors to propose that no or only very crude positional information about the presaccadic display is stored across the saccade (Bridgeman, van der Heijden, & Velichkovsky, 1994). Further findings also support the assumption that only high-level, abstract visual information is retained in transsaccadic memory. So, transsaccadic changes of the size of objects and transsaccadic changes from small to capital letters did not affect object or word naming (McConkie & Zola, 1979; Rayner, McConkie, & Zola, 1980).

In contrast to these findings, the study of Deubel, Schneider, and Bridgeman (1996) suggested that very precise position information from the previous fixation is available after the saccade, but that it can be used only under certain conditions. In this study,

subjects had to saccade to a small target that appeared in the periphery. In some trials, the target was displaced during the saccade, but remained on the display. In other trials, the target was blanked for a time interval that ranged between 0 and 250 ms, and reappeared at a displaced position. It turned out that in the blanking condition, that is when no visual information about the target location was available in a critical temporal period immediately after the end of the saccade, participants were considerably more sensitive to transsaccadic target displacements. This phenomenon was termed the “blanking effect”.

According to Deubel et al. (1996), this finding indicates that the absence of position information at the end of the saccade allows the visual system to use extraretinal signals and information about the egocentric target location stored in transsaccadic memory in order to compute a veridical prediction of the postsaccadic target location. If, however, visual information is present at the end of the saccade, the stored position information is not considered for perceptual localisation. Instead, the visual system uses the visual information that it finds after the eye movement, by relying on the “built-in assumption“ that the visual world does not change during the saccade. Given the short durations of saccadic eye movements, this null-hypothesis of visual stability is certainly a very reasonable assumption which is correct in most cases.

It also turned out that the presence of a stimulus after the saccade largely determines whether other objects in the field are seen as stable or as displaced across the saccade. This was demonstrated in experiments with two stimuli, a target and a distractor (Deubel, Bridgeman, & Schneider, 1998). One of the manipulations included a short intraand postsaccadic blanking of one of the stimuli, while the other stimulus was displaced during the saccade. Even when the blank was very short (e.g., 50 ms), the blanked object was perceived as moving across the saccade, while the moved (but continuously present) object was perceived as stable. This was true whether the object had originally been defined as the saccade goal or as the distractor. The fact that this striking illusion even occurred for object displacements of up to half of the size of the saccade illustrates that under these conditions perceptual stability is determined not by extraretinal signals, but by the object that is found when the eyes land – this object serves as a spatial reference. The blanked object is then seen as displaced because its position is judged relative to the landmark object, whose position is assumed to be stable.

The role of landmarks was elaborated further in the study by Deubel, Schneider, and Bridgeman (2002) showing that what is stored in transsaccadic memory is the relational spatial information of the presaccadic stimulus configuration. This allocentric representation is then used, after the saccade, to generate predictions of where the stimuli should appear in the visual field. Deubel (2004) analysed the spatial range within which distractors become effective as transsaccadic references. For this purpose, landmark objects (pairs of small rectangles) were placed at various locations in the vicinity of the target. The landmark objects were present when the saccade landed, while the target was blanked for 200 ms. It turned out that the effect of landmarks is spatially selective, being highest when the distractors appear close to the target. Under these conditions, the landmarks indeed largely determined transsaccadic localisation: More than 70 % of a distractor displacement was reflected in the induced target mislocalisation. This implies that when visual structure is available close to

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the target, the efference copy signal of eye position after the saccade plays only a minor role in transsaccadic localisation; rather, transsaccadic displacement judgements and perceived visual stability are based on the evaluation of postsaccadic landmark objects. The effect of the landmark falls off within 2–3 of visual angle away from the target.

Thus, it seems that landmark objects found when the eyes land after a saccade are of fundamental importance for the transsaccadic localisation of targets. The present investigation extends the previous findings by studying in more detail the relative contribution of allocentric and egocentric information stored across the saccade, and the way how the postsaccadic information is integrated with the stored representations

1. Experiment 1

As discussed before, previous findings suggested that both allocentric and egocentric representations of target position are stored across the saccade and interact in the process of postsaccadic localisation. In Experiment 1, we investigated the spatial range in which the presentation of a postsaccadic distractor would dominate the localisation of the target. For this purpose, participants were asked to saccade to a spatial arrangement of a saccade target and a distractor. The distractor was displaced during the saccade, and we determined the effect of the size of this displacement on the localisation of the (temporarily blanked) target.

1.1. Method

The stimuli were presented on a 21 video-monitor at a frame rate of 100 Hz. Screen background luminance was 2 2 cd/m2; the luminance of all presented stimuli was 25 cd/m2. The participants viewed the display binocularly from a distance of 80 cm. Head movements were restricted by a chin and forehead rest. Eye movements were measured with an SRI Generation 5.5 Purkinje-image eye-tracker (Crane & Steele, 1985) and sampled at a rate of 400 Hz. Further details of computer control, calibration, and triggering of the saccade-contingent display change are given in Deubel et al. (1996).

As shown in Figure 1a, each block started with the presentation of a fixation cross (size: 0 2 ). After a random delay of 500–1000 ms the fixation cross-disappeared, and a peripheral target appeared together with a distractor. The target was similar in size and shape to the fixation cross and was always presented on the horizontal meridian at a distance of 6 to the left or the right of the current fixation. The distractor was a vertically elongated rectangle (size: 0 11 × 0 22 ). It appeared directly above the target, at a vertical distance of 0 5 from the horizontal meridian.

Triggered by the onset of the saccade, the distractor was displaced horizontally, either in the same or in the opposite direction of the initial target step. Displacement size D varied randomly between −1 6, −0 8, 0, +0 8, and +1 6 , where positive values indicate an onward displacement, that is a shift in the direction of the saccade, while negative values indicate a backward shift. Moreover, starting with the time of saccade onset, the target was blanked for 100 ms and reappeared with a displacement T from the presaccadic target position.

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perceived transsaccadic target displacements Tperc (see Figure b). Both the size of Tperc and the displacement size T of the target are measured with respect to the position where the target initially appeared. If, as we anticipated from the former findings, participants would expect the target to reappear after the saccade in alignment with the distractor, then the value of Tperc should be found to be equal to the distractor displacement D.

At the end of each trial the participant’s task was to report, by pressing one of two buttons, whether the intrasaccadic displacement of the saccade target had occurred in the same or the opposite direction to the initial target step (forward or backward displacement). The final target position served as the starting position for the next trial. Depending on whether the final target position was rather at the centre or close to the right or left border of the display, the initial target step of the next trial could occur into the same or into the opposite direction of the previous saccade.

Each of the 25 different postsaccadic target–distractor arrangements was presented six times per experimental block, in a random order. We did not distinguish between trials with leftward and rightward initial steps; the data from these symmetrical conditions were averaged in the data analysis. Each participant performed six blocks (including 900 trials), distributed over two days. Six paid participants (5 female, 1 male) participated in the experiment. All participants had normal vision or vision that was corrected to normal by contact lenses. Their age ranged from 23 to 25 years. The participants were naive with respect to the aim of the study, but were experienced with the laboratory equipment from other eye-movement-related tasks.

1.2. Results

We excluded from the analysis all trials in which the eye-tracker registered an eye blink or lost the participant’s pupil. Also, the trials in which saccadic latency was below 140 ms or above 400 ms were discarded from further analysis. This amounted to 2.7% of all trials (146 trials).

Figure 1b displays what participants perceive in this task, dependent on the size and the direction of the intrasaccadic distractor shift. The graph shows the percentage at which participants indicate a forward displacement of the target as a function of the size of the actual intrasaccadic target shift T , and for the five different distractor displacements D. In order to obtain a measure for the perceived target displacement that was induced by the distractor manipulation, we fitted, for each of the five distractor displacements, a cumulative Gaussian function to each set of data points and then computed the thresholds (for a criterion level of 50% .1 These values are indicated by the vertical arrows in the

1 We used a bootstrap procedure to estimate the induced target mislocalisation. This “C” weighted linear regression, a cumulative Gaussian psychometric function to a set of binary data. It then computes the threshold (for a given criterion level of performance) and the gradient. The bootstrap procedure is similar to that given by Foster & Bischof (1991), but a more robust procedure has been adopted in that standard deviations are co-program is freely available from http://www.cs.ualberta.ca/ wfb/software.html. It fits, by computed from centiles, assuming a normal distribution.

200 C. Koch and H. Deubel

figure and signify the perceived target displacement induced by the distractor shift; in other words, they represent the spatial target positions at which the participants would have seen a perfectly stable target.

The relative horizontal displacements of the five psychometric functions in Figure 1b clearly demonstrate that the intrasaccadic distractor shift has a dominant effect on perceived target displacement. So, when the distractor is shifted forward by 1 6 , the psychometric function is displaced by about 1 2 in the forward direction. This indicates that the participant experiences a quite dramatic illusion: In order to be perceived as stable, the target has now to move by about 1 2 , in the same direction as the distractor shift! A one-way ANOVA confirmed a significant effect of the postsaccadic distractor position on perceived target displacement, F 4 20 = 99 984 p < 0 001.

The diamonds in Figure 1c show the means of the induced subjective target displacements Tperc, as calculated from the psychometric functions for the different intrasaccadic distractor shifts. The small dots indicate the individual values for each of the six participants. The postsaccadic distractor positions are indicated by the vertical rectangles. Note that here and in the following data graphs, the dependent variable is represented on the x-axis for illustrative purposes. The graph also displays the regression line through the data points, yielding a slope of 0.80 and a value of the correlation coefficient r of 0.98. The slope of this regression line is a direct measure of the effectiveness of the distractor in this task, describing the extent to which a certain distractor displacement results in a perceived target displacement. For this experiment, the result indicates that a distractor displacement of 1 will lead to an induced target mislocalisation of 0 8 .

The high correlation coefficient suggests that the relation between the size of the intrasaccadic distractor displacement and the induced illusion is largely linear. In order to test for linearity, we computed a one-way ANOVA with an unknown population parameter. The ANOVA yielded a non-significant deviation of the data from the linear regression, F 3 25 = 1 56; p = 0 223. This implies that, independent of the size of the intrasaccadic distractor displacement, the size of the induced target shift as perceived by the participant is always around 80% of the distractor displacement. Thus, at least for the range of distractor displacements tested in the experiment (±1 6 which is ±26 6% of the saccade amplitude), the efficiency of the postsaccadic distractor to act as a spatial landmark was constant.

The results from this experiment confirm our previous findings that a distractor which appears close to the saccade target, though irrelevant for the participant’s task, acts as a highly efficient landmark for the transsaccadic localisation of the target (Deubel, 2004). When the target is blanked after the saccade, the target location is evaluated with reference to the continuously present distractor. Quantitatively, the results also agree well with the efficiency of landmarks as analysed by Deubel (2004) for smaller distractor displacements. In this former study, two vertical lines appearing collinearly above and below the target were used as landmarks. The data analysis was similar to the one applied here and yielded a distractor efficiency of 0.73.

This experiment demonstrates that, at least within the range of ±1 6 around the presaccadic target positions, continuously presented distractors are highly efficient as landmarks.

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This indicates that allocentric information about the presaccadic target–distractor configuration is important in postsaccadic localisation: A blanked target is expected to reappear at the same relative location with respect to distractor as in the presaccadic configuration. Also, the results show that the null-hypothesis of stability of the visual world holds also in the present task; the continuously present object (the distractor) is, by default, taken as stable; therefore, it acts as a landmark. However, note that the assumed process of landmark-based localisation requires the visual system to re-identify the landmark in the postsaccadic display in order to allow for an unambiguous mapping of preand postsaccadic information. In the next experiment, we study a situation in which an unequivocal mapping of preand postsaccadic information is no longer possible. For this purpose, the presaccadic distractor was replaced by two spatially separate stimuli, visually identical to the presaccadic distractor.

2. Experiment 2

In Experiment 2, a discrepancy between the preand postsaccadic stimulus layout was introduced by presenting, after the saccade, two spatially separate distractors instead of one, with similar visual features as the presaccadic distractor. As in Experiment 1, we asked how the distractor configuration would affect the transsaccadic localisation of the saccade target. We had three possible hypotheses about the effect of the mapping ambiguity: (1) As a first possible scenario, the introduced inconsistency between preand postsaccadic information due to the appearance of the additional object in the postsaccadic scene could potentially lead to the rejection of the null-hypothesis (of a stable world), just like in simpler tasks in which no target is found due to blanking (Deubel et al., 1996). Similar to the blanking paradigm, the visual system would then possibly use a stored egocentric representation of the target position and an efference copy of the eye position for postsaccadic target localisation; as in the blanking experiments, this would result in a higher sensitivity to detect the veridical intrasaccadic target displacement.

(2) Alternatively, the visual system could possibly use the one of both distractors as a landmark that is found closer to the original target position, or closer to the landing position of the eyes. (3) Finally, it is possible that both distractors may be considered with equal weights in the task; in this case the induced target motion should result from a geometrical centre of both postsaccadic stimuli.

2.1. Method

The experimental procedure is displayed in Figure 2a. The presaccadic display and the timing of the presentation were identical to Experiment 1. Now, however, triggered with the onset of the saccade and simultaneous with the target blanking, the presaccadic distractor line was replaced by a pair of lines, both visually identical to the presaccadic distractor. The two lines had a horizontal spatial separation of 1 6 . The postsaccadic distractor pair was presented at various spatial positions which, for convenience, are depicted by the

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2.2. Results

Of all trials (353 trials), 4.9% were excluded from the analysis because the eye-tracker registered an eye blink or lost the participant’s pupil, or because saccadic latency was below 140 ms or above 400 ms.

As in Experiment 1, we first analysed the perceived direction of target displacement as a function of the position of the postsaccadic distractor (given as the spatial centre of the pair of lines). Figure 2b displays the participants’ percentage of “forward“ judgements for each of the distractor displacements, and the psychometric functions fitted through the data points. The relative displacements of the curves with varying distractor displacement D clearly demonstrate that the position of the postsaccadic distractor pair had a strong effect on the location where the target was expected to reappear. Obviously, the first of our hypotheses that, due to the ambiguity of the mapping of preand postsaccadic information, the visual system would ignore the distractor and judge the target position independently was not confirmed.

In order to analyse whether the perceived target shift would be predominantly determined by one of the two distractor lines (as assumed in hypothesis 2), we quantitatively determined, as in the previous experiment, the amount of induced target mislocalisation for each value of D by means of a bootstrap procedure. The result is plotted in Figure 2c. In this graph, the locations of the two distractor lines (relative to the presaccadic target/distractor position) are displayed by the small vertical bars.

A repeated-measures one-way analysis of variance confirmed a significant effect of the factor distractor displacement D on the perceived target displacement Tperc, F 4 28 = 72 416 p < 0 001. If, as assumed in hypothesis (2), postsaccadic localisation were largely determined by the distractor line that appeared closest to the presaccadic target position, then the postsaccadic target should be localised at the position of one of the two distractor lines. For example, for the case where the pair of lines appeared at 0 and +1 6 , perceived target displacement should be 0. Obviously, this is not the case. Rather, the data reveal that both distractors contribute about equally to the induced effect: Participants now perceive an induced target displacement which is in between both line locations. Distractor effectiveness can again be determined by computing the linear regression through the data. If both distractor lines would contribute with equal weights and would completely determine postsaccadic localisation, we would expect the induced target shifts to be equal to D, that is, the target should be relocalised at the geometrical centre of the distractors. This prediction is indicated by the dashed line, having a slope of 1. As in the first experiment, the data, however, reveal that the effectiveness of the distractor is incomplete, yielding a slope smaller than 1. The solid line in the graph displays this regression line; analysis yields a slope of 0.71, an intercept of 0.23, and a correlation coefficient r of 0.87. This indicates that, for the present condition with two postsaccadic distractor lines, about 71% of the size of the intrasaccadic distractor displacement is reflected in the induced target shift. This value is in perfect agreement with previous reports for a single distractor (Deubel, 2004), and close to the value of 80% as found in the first experiment. Additionally, the intercept of 0.23 indicates that both distractor lines are not equally