Center for Sensorimotor Research, Department of Neurology, Klinkum Grosshadern, Ludwig-Maximilians University, 81377 Munich, Germany
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ABSTRACT |
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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.
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INTRODUCTION |
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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.
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METHODS |
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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 markerimmediately 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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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.
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RESULTS |
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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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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).
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DISCUSSION |
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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.
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ACKNOWLEDGMENTS |
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We thank J. Benson for copyediting the manuscript.
This study was supported by the Deutsche Forschungsgemeinschaft (Klinische Forschergruppe BR 639/5-3).
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FOOTNOTES |
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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.
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REFERENCES |
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