Relation Between the Metrics of the Presaccadic Attention Shift and of the Saccade Before and After Saccadic Adaptation

J. Ditterich, T. Eggert, and A. Straube

Center for Sensorimotor Research, Department of Neurology, Klinkum Grosshadern, Ludwig-Maximilians University, 81377 Munich, Germany


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Ditterich, J., T. Eggert, and A. Straube. Relation Between the Metrics of the Presaccadic Attention Shift and of the Saccade Before and After Saccadic Adaptation. J. Neurophysiol. 84: 1809-1813, 2000. A shift of the visual attention focus is known to precede saccades. However, how the metrics of both this presaccadic attention shift and the saccade are coupled is still unclear. We altered the saccade size by short-term saccadic adaptation to determine whether the attention focus would still be shifted to the location of the saccade target or to the modified postsaccadic eye position. The results showed that saccadic adaptation had no influence on the presaccadic attention shift. Thus either different processes determine the metrics of the attention shift and of the saccade or saccadic adaptation causes only modifications on a lower hierarchical level of saccade programming, thereby not influencing the metrics of the attention shift.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The concept of attention has become increasingly important during the last decades. Attention is thought to allow preferential processing of a visual stimulus, if it is directed toward the location of the stimulus (Castiello and Umilta 1990; Eriksen and Webb 1989). This may explain why the reaction time to a visual stimulus is reduced, if it appears at an expected location (Posner 1980). Advance knowledge of this location allows the attention focus to be shifted there prior to stimulus onset. Several authors have suggested that attention also plays an important role in pattern recognition (Fukushima 1986; Olshausen et al. 1993). Recognition performance was shown to be best when a pattern is presented near the location of the saccade target immediately prior to a saccade (Deubel and Schneider 1996; Hoffman and Subramaniam 1995), a fast eye movement for foveating an object of interest. This implies that saccades are preceded by a shift of the attention focus to the location of the saccade target.

To determine how the metrics of both the attention shift and the saccade are coupled, we investigated the relation between the final location of the presaccadic attention shift and the postsaccadic eye position before and after manipulating the saccade size by short-term saccadic adaptation (McLaughlin 1967). A systematic intrasaccadic displacement of the saccade target induces a postsaccadic visual error, which is compensated for by a gradual adjustment of the saccade size. It is still a matter of debate where this modification takes place. The above-described procedure produces a dissociation between the initial location of the saccade target and the final eye position. Our aim was to determine whether the change in saccade size is reflected in the presaccadic attention shift or, in other words, whether the attention focus is shifted to the saccade target or to the final eye position in the adapted state. In a setup similar to that of Deubel and Schneider (1996) pattern recognition was used to probe the location of the attention focus. The recognition performance was determined at four locations relative to the saccade target before and after adaptation. A pair of patterns was always presented: a discrimination pattern at the probed location and a distracter at another location with a fixed distance.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Seven subjects (6 males, 1 female, mean age: 31 yr, age range: 26-36) with full visual acuity took part in the study. All were volunteers and gave their informed consent. Most of the subjects had previous experience in oculomotor or visual experiments, but six of them were naive as regards the purpose of the experiment. The protocols were institutionally reviewed and approved.

The subjects sat in a dark room with their head on a chin rest. Instructed not to move their head, they looked at a computer screen (NEC MultiSync 5D; size: 40 × 30 cm) located 60 cm in front of them. The video signal had a resolution of 1280 × 1024 pixels at a frame rate of 60 Hz. The background luminance of the screen was chosen relatively high to minimize effects of phosphor persistence. The horizontal eye position was measured using an infrared reflection device (IRIS, Skalar Medical BV; resolution: 2 min arc) and digitized at a sampling rate of 1 kHz.

The subjects were asked to fixate in between a pair of horizontal bars (see Fig. 1), which stepped to the left or to the right by 6 deg to trigger a saccade. The maximum eccentricity was 12.5 deg. Two patterns, 1.2 deg apart, were presented approximately 100 ms before saccade onset. The size of the patterns and the eight possible locations with respect to the target can be seen in Fig. 1. One of these two patterns was always a discrimination pattern (one of two possibilities; see Fig. 1); the other one was always a distracter. The discrimination pattern could appear at four different positions (with equal probability): at 5.1 deg retinal eccentricity (relative position: 0.85), at 5.7 deg (0.95), at 6.3 deg (1.05), and at 6.9 deg (1.15). As it was also equally likely that the discrimination pattern was the more central one or the more peripheral one of the two patterns, there were four more possible locations for the distracters. Since saccade latency can vary between subjects and during the experiment, it was measured on-line, and the time of the onset of the patterns was adjusted appropriately (with a low-pass characteristic). The exact timing on the screen was registered by optically recording the onset of a marker that appeared at the same time as the patterns but was hidden from view. A photovoltaic cell with a response time of 3 us (Siemens BPY 11) was used. Figure 2A shows the actual distribution of the onset time of the patterns with respect to saccade onset. Approximately 60 ms later the patterns were covered by a mask. The offset of the marker---immediately after completion of the mask---was recorded as a temporal upper limit for the masking. Trials in which this event was detected after saccade onset were discarded from the analysis, thereby ensuring that the patterns were completely masked when the eyes began to move. Figure 2B shows the actual distribution of the time span from marker onset to marker offset (upper limit for the presentation time of the discrimination pattern). The mask disappeared at the latest during the saccade. Beginning with the 101st primary saccade, the saccade target was displaced by 1.5 deg in the direction opposite to the primary target step as soon as a saccade was detected (eye velocity >100 deg/s) to induce adaptation. After the saccade the subjects had to decide which of the two possible discrimination patterns had been presented. They had to give their answer within 2.5 s by moving a joystick in one of two possible directions. Figure 3 shows the temporal structure of the experiment.



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Fig. 1. Geometrical structure of the experiment. The solid arrow indicates the primary step of the saccade target, the dotted arrow the secondary step occurring during the saccade to induce adaptation. The dotted bars indicate the position of the saccade target after the back step, which occurred only after the first 100 trials. Only the borders of the mask are shown to demonstrate the size and the possible locations of the patterns. The discrimination pattern was presented at one of the four probed positions. The distance between the two patterns shown simultaneously (a discrimination pattern and a distracter) was always 1.2 deg. Only the situation for saccades to the left is shown. The experiment was designed symmetrically. Saccades to the right were requested with equal probability.



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Fig. 2. A: actual distribution of the time of pattern onset with respect to saccade onset. B: actual distribution of the time span between the appearance of the patterns and the completion of the mask.



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Fig. 3. Temporal structure of the experiment.

We first recorded 50-100 fixations in the range from -15 deg to +15 deg for calibrating the eye movement data using a 3rd-order polynomial. This procedure results in an accuracy of better than 0.5 deg. Afterward the subjects were allowed 50 trials to practice the task before 300 trials were recorded. The data from the first 150 trials is called "before adaptation," and the data from the second 150 trials, "after adaptation."

In the off-line analysis saccades were marked automatically by selecting candidates with a minimum peak velocity of 50 deg/s, a maximum peak velocity of 700 deg/s, a minimum amplitude of 3 deg, a maximum duration of 150 ms, a minimum latency of 25 ms, a maximum latency of 800 ms, and reasonable main sequence parameters. The start of the saccade was marked by beginning at the peak velocity and going backward in time until the velocity dropped below 10% of the peak velocity. Likewise, the end of the saccade was marked by starting at the peak velocity and going forward in time until the velocity dropped below 10% of the peak velocity. The saccade amplitude was defined as the difference in eye position between both marks. The saccade gain is the saccade amplitude divided by 6 deg.

To present and analyze the saccade data in as close as possible to the way we did the pattern recognition data (where we had the recognition rate for different locations of the discrimination pattern with a spatial resolution of 0.6 deg), we calculated histograms with the same spatial resolution for the saccade gain for each subject.

The data from each subject had to meet the following criteria. First, the saccade gain in the second half of the experiment had to be significantly smaller than in the first half of the experiment (U test; P <=  0.05), indicating that the adaptation was successful. Second, the recognition performance had to be significantly above chance level (calculated using the binomial distribution; P <=  0.05) for at least one of the four probed positions before and after adaptation.


    RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The circles connected by the broken line in Fig. 4A show the recognition performance before adaptation as a function of the position of the discrimination pattern relative to the saccade target. The recognition rate depended significantly on the position [P = 0.02; repeated measures (RM) ANOVA] and was best at a location slightly more peripheral than the saccade target. The performance at 1.05 was significantly better than the performance at 0.95 (P = 0.05; planned comparison), revealing a tendency of the attention shift to overshoot the saccade target. The average saccade gain (saccade size divided by the amplitude of the primary target step) was 0.91. The circles connected by the broken line in Fig. 4B show the gain distribution averaged across subjects. An RM-ANOVA revealed that this distribution was not flat (P = 0.02). The adaptation led to a significant reduction of the saccade gain by 0.09 (P < 0.001; t-test for dependent samples). The circles connected by the solid line (Fig. 4B) show the average gain histogram after adaptation. An RM-ANOVA revealed that the gain distribution was significantly altered (P = 0.006). Nevertheless, the pattern of recognition performance was not significantly altered (P = 0.87; RM-ANOVA). The circles connected by the solid line (Fig. 4A) show that the peak was still at 1.05. The change in recognition performance at 0.85 was not significant (P = 0.16; t-test for dependent samples).



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Fig. 4. A: dependency of the recognition performance on the position of the discrimination pattern relative to the saccade target before and after adaptation. The abscissa shows the eccentricity of the probed position divided by the eccentricity of the saccade target. The ordinate shows the percentage of correctly identified discrimination patterns (50% = chance level). The circles represent the mean recognition rate at a certain location; the error bars show the standard error between subjects. Despite the significant gain change induced by saccadic adaptation there was no comparable change in the pattern of recognition performance. B: distributions of the saccade gain before and after adaptation. The circles show the mean relative frequency of saccade gains in an interval with a size of 0.1 centered around the horizontal position of the circle. The error bars represent the standard error between subjects.

The experimental design ensured that the distribution of the position of the discrimination pattern within the pair of patterns (left versus right and closer to the fovea versus more eccentric) was not significantly different for different positions relative to the saccade target (controlled by RM-ANOVAs; P >=  0.24).


    DISCUSSION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

During the second 150 trials we observed a discrepancy between an altered distribution of the saccade gain induced by saccadic adaptation and a not significantly altered pattern of presaccadic recognition performance. Of course, this observation does not exclude the possibility of a long-term change. However, if one restricts oneself to the observation time, the alteration of the saccade size by short-term saccadic adaptation does not change the final location of the presaccadic attention shift. The attention focus is still shifted to the location of the saccade target, not to the final eye position. There are two possible explanations for this finding.

One possibility is that the attention shift and the execution of the saccade are not based on the same metrical information. Thus changing the saccade size by adaptation would not alter the metrics of the attention shift. This could mean that shifting the attention and programming a saccade are basically two independent processes, which are only temporally coupled. The finding of Paprotta et al. (1999) that manual pointing is also coupled with an enhanced pattern recognition performance at the location of the pointing target supports the view that the attention shift is not unique to the execution of saccades. Thus a target selection process involving an attention shift could precede any kind of goal-directed action.

The second possibility is that the metrics of the attention shift and the saccade size are coupled, but that saccadic adaptation operates on a lower hierarchical level and thus does not influence the metrics of the attention shift. It is still an open question as to what is modified by saccadic adaptation. The observations that adaptation is much faster in humans than in monkeys (approx. by a factor of 10; Ditterich et al. 1999; Fuchs et al. 1996; Miller et al. 1981; Straube et al. 1997) and that a visual misperception has been reported after adaptation (Moidell and Bedell 1988) support the idea that higher-level processes could be involved. However, it seems doubtful that there is a transfer from saccadic adaptation to pointing movements, which would indicate the modification of a central target representation (Kröller et al. 1999).

Another interesting result was the tendency of the attention shift to overshoot the target in contrast to the tendency of saccades to undershoot the target. This finding again points to a dissociation between the metrics of both the attention shift and the saccade. Contrary to our results, Deubel and Schneider (1996) reported no overshoot, but an almost symmetrical decay of the performance around the saccade target. The crucial point here could be that they predefined the possible pattern locations and the size of the pattern by a mask that was present when the saccade was requested. Thus the attention could have focused on the element of the mask at the target position. In our experiment the saccade target was defined by only two bars with nothing in between. The two bars may have been insufficient to visually guide the attention focus. It is possible that the tendency of the attention shift to overshoot the target can be observed only in situations with restricted visual information at the target location.

The important finding of our study is that the visual attention focus is presaccadically shifted to the location of the saccade target and not to the landing position of the saccade. We have previously shown that the attention focus serves as a selection mechanism for the visual information used for a transsaccadic comparison to drive saccadic adaptation (Ditterich et al. 2000). We hypothesize that the presaccadic attention shift is used to code visual information about the saccade target for postsaccadic reidentification. It is therefore important that the attention is shifted to the saccade target and not to the landing position of the saccade, if there is a discrepancy between the locations.


    ACKNOWLEDGMENTS

We thank J. Benson for copyediting the manuscript.

This study was supported by the Deutsche Forschungsgemeinschaft (Klinische Forschergruppe BR 639/5-3).


    FOOTNOTES

Address for reprint requests: J. Ditterich, Center for Sensorimotor Research, Marchioninistr. 23, 81377 Munich, Germany (E-mail: ditterich{at}nefo.med.uni-muenchen.de).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 1 March 2000; accepted in final form 20 June 2000.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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