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Research Article  |   January 2005
Inhibition of saccade and vergence eye movements in 3D space
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Journal of Vision January 2005, Vol.5, 1. doi:10.1167/5.1.1
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      Olivier A. Coubard, Zoï Kapoula; Inhibition of saccade and vergence eye movements in 3D space. Journal of Vision 2005;5(1):1. doi: 10.1167/5.1.1.

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Abstract

Inhibitory capacity was investigated by measuring the eye movements of normal subjects asked to fixate a central point, and to suppress eye movements toward visual distracters appearing in the periphery or in depth. Eight right-handed young adults performed such a suppression or distracter task. In different conditions, the distracter could appear at 10° left or right at a distance of 20, 40, or 150 cm (calling for horizontal saccades), or in a central position far or close (calling for convergence or divergence), or 7.5° up or down at 40 or 150 cm (calling for vertical saccades). Eye movements were recorded binocularly with an infrared light eye-movement device. Results showed that (1) suppression performance was not perfect, as the subjects still produced eye movements; (2) errors were distributed unequally in three-dimensional space, with more frequent errors toward distracters calling for convergence, or leftward and downward saccades at a close distance; (3) distracters calling for saccade suppression yielded saccades in the direction of the distracter (that we called prosaccades), and saccades directed away from it (that we called spontaneous antisaccades); (4) for vergence, only distracters calling for convergence yielded errors, which were always promovements; (5) in addition, a small convergent drift was found for convergence distracters. Differences in the errors between saccade and vergence suggest that different inhibitory mechanisms may be involved in the two systems. Spatial left/right, up/down, and close/far asymmetries are interpreted in terms of attentional biases.

Introduction
Ocular fixation is the ability to keep the eyes stable on the object foveated. The object can be present (visual fixation) or absent. In the latter case, the fixation is memory-guided as the subject voluntarily holds his/her gaze on the remembered location of the object. Since Dodge (1907), visual fixation has been extensively studied, and several types of micro-phenomena have been described: tremor, drifts, and microsaccades (Leigh & Zee, 1999; Martinez-Conde, Macknik, & Hubel, 2004; Yarbus, 1967). Nonspecific to and fro saccadic eye movements, called square-wave jerks (SWJ) because of their particular pattern, have also been observed in normal subjects (Elidan, Gay, & Lev, 1984; Shallo-Hoffmann, Sendler, & Mühlendyck, 1990). Ohtsuka, Mukuno, Ukai, and Ishikawa (1986) proposed a continuum between microsaccades and SWJ that would vary just in amplitude and would reflect normal physiological instability of ocular fixation. The debate about the role of fixational eye movements in visual perception was revived in the last few years. Contrary to Kowler and Steinman (1979) but in line with Ditchburn (1980), an increasing number of studies showed that microsaccades are essential for vision. Particularly, electrophysiological recordings of neural responses in several visual areas of the monkey showed that microsaccades prevent the fading of visual perception by refreshing the retinal images (for a review, see Martinez-Conde et al., 2004). Cognitive processes can modulate fixational eye movements. The occurrence and amplitude of the different eye movements occurring during a fixation task have been found to increase with increasing attentional demands (Kowler, 1991; Shaffer, Krisky, & Sweeney, 2003). Similarly, the oculomotor instability in memory-guided fixation was found to be increased by comparison with visual fixation (Kowler, 1991; Leigh & Zee, 1999; Smyrnis et al., 2003). Recently, the amplitude and direction of microsaccades were found to be modulated by attention: The microsaccades would constitute an overt measure of covert attention shifts (Engbert & Kliegl, 2003; Hafed & Clark, 2002). 
The suppression task is an attentional paradigm asking the subject to keep his eyes fixating the location of the fixation point, and ignoring distracters appearing in the periphery (i.e., suppressing or inhibiting eye movements toward them). In the suppression task, the fixation can be either visual or memory-guided. Fukushima, Fukushima, Morita, and Yamashita, (1990) reported a high rate of unwanted saccades in many of their schizophrenic patients performing a visual fixation task, in the presence of flashed distracters. Most saccades observed in these clinical studies were reflexive (i.e., showing express latencies between 80 and 120 ms). Smyrnis et al. (2003) studied normal subjects and found increased saccade frequency in a visually guided fixation task when distracters were flashed at the periphery, by comparison with a fixation task without distracters. Saccade suppression tasks have been used in a positron emission tomography (PET) study by Law, Svarer, Holm, and Paulson (1997), who reported brain activity mainly in the right hemisphere. Consistently, Tzelepi, Lutz, and Kapoula (2004) showed that EEG activity was enhanced on the right hemisphere in subjects asked to suppress saccade or vergence eye movements. 
Another task that involves suppression or inhibition is the antisaccade paradigm (Hallett, 1978). In this task, after the extinction of a central fixation point (FP), a target appears in the periphery and the subject is instructed to look at the opposite side. As in studies of prosaccades, the temporal relationship between the offset of the FP and the onset of the target may be simultaneous (the target appears simultaneously with the FP offset), gap (a time interval is introduced between the FP offset and the target onset), or overlap (the FP remains on when the target appears). The task may also be memory-guided (e.g., see Kapoula, Bucci, Bernotas, & Zamfirescu, 2000). In the antisaccade task (mostly gap), a high rate of erratic prosaccades toward the stimulus was reported in subjects with either fixation and/or inhibitory abilities in immature children (Fischer, Biscaldi, & Gezeck, 1997a) or impaired in express saccade makers (Biscaldi, Fischer, & Stuhr, 1996; Cavegn & Biscaldi, 1996). Antisaccade deficit was also observed consecutively to a lesion of the dorsolateral prefrontal cortex (DLPFC) (Pierrot-Deseilligny et al., 2003a; Pierrot-Deseilligny, Rosa, Masmoudi, Rivaud, & Gaymard, 1991) or of the anterior cingulate cortex (Gaymard et al. 1998; Milea et al., 2003). Similar defect has been reported in Huntington’s disease (Lasker, Zee, Hain, Folstein, & Singer, 1987; Rothlind, Brandt, Zee, Codori, & Folstein, 1993), progressive supranuclear palsy (Blin et al., 1995; Pierrot-Deseilligny, Rivaud, Pillon, Fournier, & Agid, 1989), and schizophrenia (for reviews, see Everling & Fischer, 1998; McDowell & Clementz, 2001). Brain imaging studies revealed a widely distributed neural network during the antisaccade performance (for a review, see Munoz & Everling, 2004). 
The aim of the present study was to measure the ability of normal subjects to inhibit eye movements in a suppression task. In a gap paradigm, a distracter appeared in different locations in three-dimensional (3D) space, on the left or on the right, up or down, at close or at far. The movement to suppress could be a saccade, either lateral or vertical, or vergence, either convergence or divergence. We expected the suppression performance not to be perfect, and the errors to be distributed heterogeneously in 3D space, depending on spatial attentional allocations. Such expectations were partially based on prior studies showing shorter saccade latencies at close than at far (Bucci, Kapoula, Yang, Wiener-Vacher, & Bremond-Gignac, 2004; Yang, Bucci, & Kapoula, 2002), and differences in EEG cortical activation for saccades and vergence (Kapoula, Evdokimidis, Smyrnis, Bucci, & Constantinidis, 2002; Tzelepi et al., 2004). 
Methods
Subjects
Eight healthy subjects (four women and four men) participated in the experiment. They were aged 22.6 ± 4.4 years (range = 19\2-31 years) and had 13.4 ± 1.2 years of education (range = 12–15 years). All were naïve to the purpose of the experiment and had never participated in eye-movement recordings. They gave their written consent and were paid for the present study, which was approved by the ethics committee and consistent with the Declaration of Helsinki. 
A brief clinical examination was performed. The handedness, assessed by Edinburgh Handedness Inventory (Oldfield, 1971), was right dominant for the group of subjects (97.0 ± 5.6%, range = 87–100%; 100% indicating absolute right-handedness). Six of the eight subjects were right eye dominant. Subjects had no neuro-ophthalmological deficit and binocular vision without correction was normal. The proximal point of convergence was 58 ± 17 mm for the group of subjects. The amplitude of convergence, measured with a bar of prisms, was for the group of subjects 22.4 ± 6.5 diopters at 20 cm and 17.3 ± 7.8 diopters at 150 cm. The amplitude of divergence was 10.4 ± 3.9 diopters and 3.6 ± 1.3 diopters at 20 and 150 cm, respectively. These values were normal (von Noorden, 2002). Stereoscopic vision, assessed by the TNO (Test of Netherlands Organization; Richmond Products, Boca Raton, FL), was normal: median of 30 arcsec (range = 15–60″). 
Apparatus
Eye positions were recorded binocularly with a Skalar Iris infrared light eye-movement device (Skalar Medical b.v., The Netherlands). As we recorded successively horizontal and vertical eye movements, the sensors had to be clipped and fixed into the frame in alternatively the horizontal or the vertical direction. The system had a bandwidth of 100 Hz and was able to measure linearly within 3% horizontal eye movements up to 25° or vertical eye movements up to 16°. The optimal resolution was 2 arcmin. Data collection was performed using REX software (available online at http://www.tchain.com by Timothy C. Hain; North-western University Medical School, Chicago, IL). Eye position signals were stored on a disk for later off-line analysis. Each channel was sampled at 500 Hz. Another computer was used to monitor the triggering of the diodes. 
For horizontal eye-movement recording, head movements were minimized by a bite board, which was attached to the table. For vertical eye-movement recording, the head was stabilized by both a chin rest and a forehead support. 
Stimuli
The subjects sat facing a table (either horizontal or vertical) in which were embedded 2.9-mm diameter red light-emitting diodes (LEDs). The subjects performed four different conditions. As the task required suppression of eye movements (see Procedure), we may refer, in the following paragraphs, either to the distracter to ignore or to the movement to suppress for the description of the spatial arrangement. The amplitudes of vergence (to suppress) were calculated considering the mean interpupillar distance for the group of subjects (61 ± 2 mm). 
For conditions 1 and 2, the horizontal table was adjusted at eye level, and the diodes were arranged on isover-gence circles at three viewing distances, 20, 40, and 150 cm. Under all conditions, the initial fixation diode was in the primary position. 
In condition 1 (see Figure 1A, left), we used six diodes. This setup is standard for the investigation of saccade and vergence in far and close space (see Bucci et al., 2004; Coubard, Daunys, & Kapoula, 2004; Kapoula, Isotalo, Müri, Bucci, & Rivaud-Péchoux, 2001; Yang & Kapoula, 2003). Three diodes were placed 150 cm away from the subject’s eyes, one in the center, and two at ±10°. The required mean angle of vergence for fixating any of these diodes was 2.3°. The other three diodes were placed at 20 cm, one in the center and two at ±10°; the mean angle of vergence was 17.0°. The fixation stimulus was either the central diode at 20 cm or that at 150 cm. Thus, this condition called for six types of movements to suppress: saccades to the left or to the right at either 20 or 150 cm and convergence and divergence between the two central diodes at 20 and 150 cm. The amplitude of the required vergence to suppress was 14.7° (17.0–2.3°) for both convergence and divergence. 
Figure 1
 
(A). Condition 1 (left): Six light-emitting diodes (LEDs) were positioned on a table at eye level. The fixation point (FP) was the central LED at either 20 cm (close) or at 150 cm (far). When the close FP was lighted on, the distracter could be (1) either one of the two lateral LEDs at 20 cm (10° version) or (2) the central LED at 150 cm (14.7° divergence). When the FP was the central LED at150 cm, the distracter could be (1) either one of the two lateral LEDs at 150 cm (10° version) or (2) the center at 20 cm (14.7° convergence). Condition 2 (middle): Five LEDs were positioned on the same table. The FP was the central LED placed 40 cm away from the subject’s eyes. The distracter LED could be (1) either one of the two lateral LEDs at 40 cm (10° version) or (2) the center one at 20 cm (8.3° convergence) or the center one at 150 cm (6.4° divergence). Conditions 3 and 4 (right): Three LEDs were embedded in the vertical plane at a viewing distance of either 40 cm (condition 3) or 150 cm (condition 4). The FP was the central LED. The distracter LED could be one of the two altitudinal LEDs (7.5° version). (B). The gap paradigm was used for the distracter task. After a fixation period varying from 2 to 2.5 s, a temporal gap of 200 ms was introduced before the appearance of the distracter. The distracter was on for1.5 s, then a beep occurred indicating the 2-s pause (the subject was in a dark room). In the no-distracter task (control), the fixation period lasted 2–2.5 s. Then, the fixation LED was switched off and no distracter appeared. A beep occurred 1.7 s after the extinction of FP to indicate the pause of 2 s. Dotted rectangles indicate the time window of interest on which the analyses were restricted.
Figure 1
 
(A). Condition 1 (left): Six light-emitting diodes (LEDs) were positioned on a table at eye level. The fixation point (FP) was the central LED at either 20 cm (close) or at 150 cm (far). When the close FP was lighted on, the distracter could be (1) either one of the two lateral LEDs at 20 cm (10° version) or (2) the central LED at 150 cm (14.7° divergence). When the FP was the central LED at150 cm, the distracter could be (1) either one of the two lateral LEDs at 150 cm (10° version) or (2) the center at 20 cm (14.7° convergence). Condition 2 (middle): Five LEDs were positioned on the same table. The FP was the central LED placed 40 cm away from the subject’s eyes. The distracter LED could be (1) either one of the two lateral LEDs at 40 cm (10° version) or (2) the center one at 20 cm (8.3° convergence) or the center one at 150 cm (6.4° divergence). Conditions 3 and 4 (right): Three LEDs were embedded in the vertical plane at a viewing distance of either 40 cm (condition 3) or 150 cm (condition 4). The FP was the central LED. The distracter LED could be one of the two altitudinal LEDs (7.5° version). (B). The gap paradigm was used for the distracter task. After a fixation period varying from 2 to 2.5 s, a temporal gap of 200 ms was introduced before the appearance of the distracter. The distracter was on for1.5 s, then a beep occurred indicating the 2-s pause (the subject was in a dark room). In the no-distracter task (control), the fixation period lasted 2–2.5 s. Then, the fixation LED was switched off and no distracter appeared. A beep occurred 1.7 s after the extinction of FP to indicate the pause of 2 s. Dotted rectangles indicate the time window of interest on which the analyses were restricted.
In condition 1, the FP could be far or close. It was of interest to study the ability to suppress eye movements when only one fixation point was required. Thus, we introduced a second condition using five diodes (see Figure 1A, middle). This setup is also standard for the investigation of saccade and vergence (see Takagi, Frohman, & Zee, 1995; Tam & Ono, 1994). The fixation stimulus was a central diode placed at 40 cm from the subject’s eyes. The mean angle of vergence for fixating this diode was 8.7°. Four distracters could be lighted, one at a time at 10° left or right (for saccades), in the center at 20 cm (for convergence), or at 150 cm (for divergence). The amplitude of the required vergence to suppress was 8.3° (17.0–8.7°) for the convergence and 6.4° (8.7–2.3°) for the divergence. 
In conditions 3 and 4 (Figure 1A, right), the subjects faced a vertical plane of LEDs. The fixation stimulus was a diode located centrally at the subject’s eyes level. Two distracters could be lighted, one at a time at 7.5° up or down. Thus, there were two eye movements to suppress in these conditions: upward and downward saccades. The condition was performed either 40 cm (condition 3) or 150 cm (condition 4) from the subject’s eyes. 
To sum up, the subjects had to suppress 14 different types of eye movements: horizontal leftward or rightward saccades at a viewing distance of 20 cm (condition 1), 40 cm (condition 2), or 150 cm (condition 1); convergence with amplitude of either 8.3° (condition 2) or 14.7° (condition 1); divergence with amplitude of either 6.4° (condition 2) or 14.7° (condition 1); and upward or downward sac-cades at a viewing distance of either 40 cm (condition 3) or 150 cm (condition 4). 
The experiment was conducted in a dark room. When all diodes were switched off, the luminance of the background of both the horizontal table and the vertical plane was 0 cd.m−2. When switched on, the minimum luminance of each diode was 0.0016 cd.m−2, which was well above the perceptual threshold. 
Procedure
In a distracter task (main condition; see Figure 1B), the central fixation diode was turned on for 2–2.5 s for each trial. The subject was instructed to fixate the stimulus as accurately as possible. Then, the fixation diode was switched off, and a distracter diode appeared 200 ms later (after the gap period). The subject was instructed to maintain his gaze on the location of the initial fixation stimulus (i.e., to fixate the remembered location of the initial fixation diode, no matter where the distracter appeared). The distracter diode stayed on for 1.5 s. A pilot study performed on ourselves revealed that the task was effortful and some-what irksome, and was likely to induce tiredness. Thus, to maintain the subject’s attention, we introduced a beep at the end of each trial, simultaneously with the distracter’s offset. The beep indicated the 2-s pause, during which the subject was invited to blink systematically to prevent fatigue effects. 
As a control condition, we used a no-distracter task (see Figure 1B) in which conditions were similar but no distracter appeared. The central fixation was turned on for 2–2.5 s. Then it was switched off and no distracter appeared. The instruction given to the subject was to fixate the remembered location of the fixation stimulus until a beep occurred. As in the distracter task, the beep indicated the end of the trial, and the subject was invited to blink systematically during the 2-s pause period. 
The design is presented in Table 1. Each subject performed several blocks. Each block contained 30–60 trials preceded and followed by calibration (see the following section). In total, each subject completed 30 trials per experimental condition. In the distracter task (see Table 1, Distracter Task), each subject performed 7 blocks: 3 blocks in condition 1, 2 blocks in condition 2, and 1 block in conditions 3 and 4. The no-distracter task was performed in separated blocks. Indeed, it was shown that mixing trials aiming to assess inhibitory abilities (e.g., antisaccade trials) with other trials different in nature (e.g., prosaccade trials) interferes significantly on the performance of both types of trials (Weber, 1995). In the no-distracter task (see Table 1, No-Distracter Task), each subject performed 4 blocks, one for each condition. The experiment lasted about 1.5 hr in all for each subject, always with a pause between 2 blocks. 
Table 1
 
Design. N indicates the number of trials within a block. FP = fixation point.
Table 1
 
Design. N indicates the number of trials within a block. FP = fixation point.
Distracter Task No Distracter Task (control)
Nb of distracters (one at a time) Nb of blocks Nb of FP (one at a time) Nb of blocks
Condition 1 (horizontal) 6 3 (N = 60) 2 1 (N = 60)
Condition 2 (horizontal) 4 2 (N = 60) 1 1 (N = 30)
Condition 3 (vertical) 2 1 (N = 60) 1 1 (N = 30)
Condition 4 (vertical) 2 1 (N = 60) 1 1 (N = 30)
Total = 7 Total = 4
The order of presentation of the conditions was counterbalanced as closely as possible. Distracter location was randomized within each block. 
Calibration
For calibration, the subjects made a sequence of saccades at the beginning and at the end of each block of the distracter or no-distracter tasks. These movements helped to keep subjects alert and attentive. 
In condition 1, the subject fixated the diodes switched on one after the other, at 0° (centrally) and 5°, 10°, 15° on the left and on the right, at 20, and at 150 cm. In condition 2, the subject fixated the diodes located at 0°, 5°, 10°, and 15° on the left and on the right at 40 cm. In conditions 3 and 4, the subject fixated the diodes located at 0°, 7.5°, and 15° upward and downward. 
Each diode remained lighted on for 1.5 s, and the recording of eye movements was performed continuously and binocularly. A polynomial calibration was established by using fixation periods lasting at least 100 ms with an error staying below 0.5°. This method provided a very reliable calibration, as indicated by an average fixation error remaining below 1°. 
Data analysis
We calculated two signals from the raw position records. A saccade or conjugate signal was calculated using the average of the calibrated left eye and right eye positions. A vergence or disconjugate signal was calculated by subtracting the right eye position from the left eye position, so convergence resulted in a positive deviation and divergence in a negative deviation. In the present study, we restricted the analysis on the conjugate signal for horizontal or vertical saccades, and the disconjugate signal for convergence and divergence. The rationale was to detect eventual movements toward or away from the direction or depth of the distracter. Erroneous movements in depth in response to direction distracters or movements in direction in response to depth distracters may happen but their analysis was beyond the scope of this study. 
For each trial, we focused the analysis on a time window reduced to a period of 1 s (indicated by a dotted rectangle in Figure 1B) and including the successive parts as follows: the last 400 ms of the fixation period, the 200 ms of the gap period, and the first 400 ms of the test period, in which the subject was instructed to fixate the remembered location of the initial fixation stimulus. The last 400 ms of fixation were considered as the baseline. The test period was reduced to the first 400 ms, which is the standard upper latency limit in adults for slow regular saccades (Fischer, Gezeck, & Hartnegg, 1997b). 
We rejected trials contaminated by blinks and those for which the fixation (the last 400 ms of fixation) was unstable. We considered the fixation as unstable when the amplitude of the position signal (either saccade or vergence) deviated over 0.5°. In all, 15.8% of the trials (range = 7.4–28.6%) were excluded from the analysis, which was consistent with a prior report (Coubard et al., 2004; 14.9% of rejection). 
We grouped the data of all subjects and performed the following two analyses. 
Analysis 1: Failure of suppression measured by pro- and anti-movements
The first step of the analysis was to investigate whether the subjects produced erratic eye movements (i.e., movements detectable by standard velocity criteria). In the present study, we called pro-movements the erratic movements in the direction of the distracter (either pro-saccades for distracters located laterally or altitudinally or provergence for distracters located in depth). When the erratic movements were directed away from the distracter, we called them anti-movements (either antisaccades or antivergence). 
In our experiment, the subjects were asked to fixate a remembered location. An important methodological issue was to determine whether the eye movements observed in our experiment were only inherent to fixational activity or related to the task demands. As mentioned in the Introduction, fixation activity has three main components: tremor, slow drifts, but also small saccades. Among the latter, SWJ are rapid, to and fro, saccadic eye movements, which form rectangular waves, with varying amplitude, frequency, and width. Shaffer et al. (2003) considered as SWJ saccades with an amplitude between 0.15 and 3° and an inter-saccades delay (time interval between the to and fro saccades) up to 400 ms (see also Discussion). Our criteria to distinguish eye movements related to our task from those occurring naturally during fixation were the following:
  •  
    Eye movements occurring after the onset of distracter were first detected by velocity criterion. The eye velocity of either conjugate or disconjugate signal was computed using a symmetrical two-point differentiator after low-pass filtering with a Gaussian FIR filter with a cut-off frequency of 33 Hz. The detection of either saccade or vergence was done automatically, and checked by the experimenter. The onset of saccades was determined at the point when the eye velocity of the conjugate signal exceeded 15°/s. The onset of vergence was determined at the point when the eye velocity of the disconjugate signal exceeded 5°/s. These criteria are standard (Coubard et al., 2004; Takagi et al., 1995).
  •  
    The minimum amplitude of the pro- or antimovements had to be 0.5°. Studies with normal subjects showed that movements with amplitude above this limit attest a failure in maintaining fixation either in the horizontal axis (Pitzalis & Di Russo, 2001; Smyrnis et al., 2003) or in the vertical axis (Pitzalis & Di Russo, 2001). As commented in the Discussion, the 0.5° limit should exclude most microsaccades.
  •  
    SWJ typically consist in a saccade away from the intended position of fixation followed, up to 500 ms later, by a return saccade to the FP (for a review, see Elidan et al., 1984). To exclude such movements, we did not select eye movements that were either preceded in the last 500 ms, or followed in the next 500 ms, by a movement in the opposite direction. For example, if the onset movement occurred 400 ms after distracter onset, we checked that no movement occurred in the opposite direction, backward for the period from −100 ms to +400 ms and forward for the period from +400 ms to +900 ms. Thus, we selected eye movements occurring singly for a time period of 1 s, which was centered on the onset of the movement. Our criterion of 500 ms for the inter-saccades interval of SWJ is also commented in the Discussion.
The effects of the type of movement, the direction of distracter, and the viewing distance on the frequencies of pro- and anti-movements were tested using Friedman ANOVA for the group of subjects; two-by-two comparisons were performed with Wilcoxon test. 
Analysis 2: Failure of suppression measured by fixation instability
Beside erratic pro- and anti-movements, it was interesting to search further for deviations in the position signal, which would drift toward the location of the distracter (or in the opposite direction), even though the movement failed to reach the velocity threshold and to elicit a clear eye movement. 
We grouped all remaining signals for the group of subjects and averaged them for both the distracter task and the no-distracter task. The group averages for both tasks were plotted together for each type of eye movement. Statistics were applied to the amplitude difference between the two tasks. For our window of interest (from −600 to +400 ms relative to the distracter onset), we divided the time into intervals of 20-ms width. Global difference between the distracter and the no-distracter tasks was tested using Friedman ANOVA. When significant, two-by-two comparisons were performed between time intervals using Wilcoxon test. 
Results
Failure of suppression measured by pro- and anti-movements
Here we report eye movements that were detected after the onset of the distracter. Using our selective criteria (see Methods), no movement was found in the no-distracter task. Thus, the movements described below only concern the distracter task. The errors were equally distributed throughout the experiment and no learning or fatigue effect was found. The following description first emphasizes the frequencies of errors (pro- and anti-movements) in the different conditions, and indicates afterward their temporal and dynamic characteristics. 
Distracters calling for lateral saccades
Figure 2 shows the trajectories and Table 2 presents the numerical values. Distracters located either leftward or rightward yielded prosaccades in all conditions (mean = 2.64%). Spontaneous antisaccades were also observed at a similar rate (mean = 2.64%). 
Figure 2
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared laterally either leftward(left) or rightward (right) at viewing distances (Vd) of 20 cm (A), 40 cm (B), or 150 cm (C). Only saccades starting 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye horizontal signals): By convention, a positive deviation indicates a rightward movement, and a negative deviation indicates a leftward movement. The amplitude of movements (in degrees) is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to distracter onset. Gaze positions are relative and were offset at time −600 ms for clarity of display. For each distracter, the occurrence of prosaccades (Pro) and that of antisaccades (Anti) is indicated in bold. We report the averages and SDs of latency (ms), amplitude (°),and peak velocity (°/s) close to the corresponding trajectories. The two vertical dotted lines delineate the gap period: the FP offset at time \t-200 ms and the D (distracter) onset at time 0 ms.
Figure 2
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared laterally either leftward(left) or rightward (right) at viewing distances (Vd) of 20 cm (A), 40 cm (B), or 150 cm (C). Only saccades starting 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye horizontal signals): By convention, a positive deviation indicates a rightward movement, and a negative deviation indicates a leftward movement. The amplitude of movements (in degrees) is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to distracter onset. Gaze positions are relative and were offset at time −600 ms for clarity of display. For each distracter, the occurrence of prosaccades (Pro) and that of antisaccades (Anti) is indicated in bold. We report the averages and SDs of latency (ms), amplitude (°),and peak velocity (°/s) close to the corresponding trajectories. The two vertical dotted lines delineate the gap period: the FP offset at time \t-200 ms and the D (distracter) onset at time 0 ms.
Table 2
 
Parameters of lateral erratic saccades. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the left/right asymmetry (L/R), and for the viewing distance (20/40/150). p < .05; ns = no significant difference.
Table 2
 
Parameters of lateral erratic saccades. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the left/right asymmetry (L/R), and for the viewing distance (20/40/150). p < .05; ns = no significant difference.
Prosaccades (2.64%) Antisaccades (2.64%) All
Frequency (%) Left Right L/R Left Right L/R
Vd=20 cm 6.67 2.50 ns 5.00 3.33 ns 4.37
Vd=40 cm 1.25 2.08 ns 4.58 0.42 * 2.08
Vd=150 cm 1.25 2.08 ns 1.67 0.83 ns 1.45
20/40/150 > ns ns ns ns *
Latency (ms)
Vd=20 cm 292(50) 249(81) 314(38) 313(41)
Vd=40 cm 264(46) 196(126) 305(54) 85(-)
Vd=150 cm 293(46) 272(39) 292(93) 343(19)
Amplitude (°)
Vd=20 cm −4.6(4.2) 4.1(4.1) 1.2(0.5) −1.1(0.4)
Vd=40 cm −6.7(4.9) 1.6(1.1) 1.2(0.5) −0.6(−)
Vd=150 cm −10.1(0.3) 7.5(3.8) 1.0(0.1) −1.1(0.4)
When pro- and antisaccades were pooled, we found a distance effect. The error rate increased significantly with decreasing viewing distance: 1.45% at 150 cm, 2.08% at 40 cm, and 4.37% at 20 cm (Chi28,2 = 6.9, p = .0323). 
The leftward distracter at 20 cm yielded the highest error rate: 6.67% of prosaccades and 5% of antisaccades (see Figure 2A, left). At 40 cm, prosaccades occurred at similar rates for leftward (1.25%) and rightward (2.08%) distracters (Z < 1). Antisaccades to leftward distracter (i.e., rightward saccades) were more frequent than antisaccades to rightward distracter (i.e., leftward saccades): 4.58% and 0.42%, respectively (Z8 = 2.0, p = .0431). At 150 cm, the error rate was low and similar for the left side and the right side. All together, these results suggest more errors when the distracter was leftward and at a close distance. The highest error rate was for the leftward distracter at 20 cm. At 40 cm, rightward saccades were the most frequent, but only in response to the leftward stimulus. 
All subjects showed prosaccades (range = 0.56–7.78%) or antisaccades (range = 0.56–5%). Nevertheless, the absence of errors for some subjects in specific conditions did not allow a statistical analysis of their parameters (latency, amplitude, velocity; see Table 2), so we comment only qualitatively. 
Almost all latencies were slow regular ones (181–400 ms; Fischer et al., 1997b). Prosaccades tended to show shorter latencies and higher amplitude than did antisaccades. However, as shown in Figure 2A, prosaccades tended to exhibit two subpopulations: A first population of saccades had a latency below 300 ms and a large amplitude; a second one had a higher latency (above 300 ms) and a small amplitude. Taken together, the amplitude of prosaccade reached at least 40% of distracter eccentricity, and it got closer to the latter with increasing viewing distances. The absolute mean was 4.3° at 20 cm, 4.15° at 40 cm, and 8.8° at 150 cm for both leftward and rightward prosaccades. 
The population of antisaccades was more homogeneous than that of prosaccades. Their latency and amplitude were similar for both sides and independent of viewing distances. The latency was in the range of that of small prosaccades (above 300 ms). The amplitude did not exceed 10% of distracter eccentricity. 
To summarize, the ability to suppress saccades toward lateral distracters was not perfect, and it led to pro- and antisaccades at similar rates. The error rate increased with proximal viewing distance, and was higher for leftward distracters, especially at close distance. 
Distracters calling for vergence
Trajectories are shown in Figure 3 and numerical values in Table 3. Recall that we differentiated four types of vergence: convergence from either 40 cm (see Figure 3A) or 150 cm (see Figure 3B) and divergence from either 40 cm (see Figure 3C) or 20 cm (see Figure 3D). 
Figure 3
 
Trajectories of pro- and antivergence observed in the distracter task only, when a distracter appeared in depth. The distracter LED could appear in front of the fixation LED, calling for a convergence from 40 to 20 cm (A) or from 150 to 20 cm (B). The distracter LED could appear behind the fixation LED, calling for a divergence from 40 to 150 cm (C) or from 20 to 150 cm (D). Only vergence starting 80 ms after distracter onset are shown. For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the vergence signal (difference between left eye and right eye horizontal signals) so that a convergence results in a positive deviation and a divergence in a negative one. Other notations as in Figure 2.
Figure 3
 
Trajectories of pro- and antivergence observed in the distracter task only, when a distracter appeared in depth. The distracter LED could appear in front of the fixation LED, calling for a convergence from 40 to 20 cm (A) or from 150 to 20 cm (B). The distracter LED could appear behind the fixation LED, calling for a divergence from 40 to 150 cm (C) or from 20 to 150 cm (D). Only vergence starting 80 ms after distracter onset are shown. For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the vergence signal (difference between left eye and right eye horizontal signals) so that a convergence results in a positive deviation and a divergence in a negative one. Other notations as in Figure 2.
Table 3
 
Parameters of erratic vergence. FP at 150/20 cm: fixation point at 150 cm for convergence and 20 cm for divergence. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the convergence/divergence asymmetry (C/D) and for the viewing distance (40/150). *p < .05; ns = no significant difference.
Table 3
 
Parameters of erratic vergence. FP at 150/20 cm: fixation point at 150 cm for convergence and 20 cm for divergence. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the convergence/divergence asymmetry (C/D) and for the viewing distance (40/150). *p < .05; ns = no significant difference.
Provergence (3.75%) Antivergence (0.62%) All
Frequency (%) Convergence Divergence C/D Convergence Divergence C/D
FP at 40 cm 8.75 0.42 * 0.42 1.25 ns 2.71
FP at 150/20 cm 5.42 0.42 ns 0 0.83 ns 1.67
40/150 > ns ns ns ns ns
Latency (ms)
FP at 40 cm 152(18) 132(−) 125(−) 170(54)
FP at 150/20 cm 164(49) 83(−) 88(6)
Amplitude (°)
FP at 40 cm 1.9(2.4) −0.7(−) −0.6(−) 0.8(0.1)
FP at 150/20 cm 3.8(6.3) −0.7(−) 0.8(0.3)
Distracters calling for convergence yielded the highest error rates (see Figure 3A–B). The errors were mostly directed toward the distracter (i.e., convergence), while antivergence divergence was either scarce or null. The vicinity of the FP and the distracter in depth tended to influence the error rate. Indeed, a convergence distracter (at 20 cm) with the eyes fixating at 40 cm yielded 8.75% convergence, while fixation at 150 cm yielded 5.42% convergence. How-ever, the difference failed to reach statistical significance (Z8 = 1.05, p = .294). 
Distracters calling for divergence yielded almost insignificant error rates (see Figure 3C–D). Only 0.42% of divergence was found, whatever the initial fixation point, and little convergence was observed. 
All subjects produced erratic provergence (range = 1.67–14.2%), but only four of the eight subjects exhibited antivergence (range = 0.83–1.67%). Thus, no statistical analysis was performed on timing and dynamic parameters. As shown in Table 3, the latencies of errors were in the range of fast regular movements (121–180 ms; Fischer et al., 1997b), and some scarce express movements could be observed. The amplitude of divergence (either pro- or antivergence) did not exceed 1°, whatever the initial point. In contrast, for distracters calling for convergence, unwanted convergence could reach the amplitude of the distracter depth (see Figure 3A–B). Nevertheless, in most convergence trials (for 71% and 77% of trials, for convergence from 40 cm and convergence from 150 cm, respectively), unwanted convergence stayed below an amplitude of 1°, which corresponds to 12% and 7% of distracter depth for convergence from 40 cm and convergence from 150 cm, respectively. 
In summary, the distracter at far calling for divergence yielded a negligible rate of errors. In contrast, the distracter at close calling for convergence was responsible for frequent errors, which were convergence. Convergence rate and amplitude tended to increase with increasing vicinity between the location to foveate and the distracter to ignore. 
Distracters calling for vertical saccades
Trajectories are shown in Figure 4, and Table 4 presents the numerical data. Compared with other types of distracters, vertical distracters yielded fewer errors (1.20%) than did lateral distracters (2.64%) or distracters in depth (2.19%). 
Figure 4
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared altitudinally either downward (left) or upward (right) at viewing distances (Vd) of 40 cm (A) or 150 cm (B). Only the saccades triggered at least 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye vertical signals): A positive deviation indicates an upward movement and a negative deviation indicates a downward movement. No pro- or antisaccades were observed for the upward distracter at 150 cm. Other notations as in Figure 2.
Figure 4
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared altitudinally either downward (left) or upward (right) at viewing distances (Vd) of 40 cm (A) or 150 cm (B). Only the saccades triggered at least 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye vertical signals): A positive deviation indicates an upward movement and a negative deviation indicates a downward movement. No pro- or antisaccades were observed for the upward distracter at 150 cm. Other notations as in Figure 2.
Table 4
 
Parameters of erratic vertical saccades. For latency and amplitude, we provide the average and the SDs in parentheses. Statistics are on frequencies only for the down/up asymmetry (D/U) and for the viewing distance (40/150). ns = no significant difference.
Table 4
 
Parameters of erratic vertical saccades. For latency and amplitude, we provide the average and the SDs in parentheses. Statistics are on frequencies only for the down/up asymmetry (D/U) and for the viewing distance (40/150). ns = no significant difference.
Prosaccades (0.94%) Antisaccades (1.45%) All
Frequency (%) Down Up D/U Down Up D/U
Vd=40 cm 0.42 2.92 ns 3.75 0 ns 1.77
Vd=150 cm 0.42 0 ns 2.08 0 ns 0.62
40/150 > ns ns ns ns ns
Latency (ms)
Vd=40 cm 249(-) 295(91) 282(39) -
Vd=150 cm 247(-) - 297(34) -
Amplitude (°)
Vd=40 cm −5.9(-) 1.8(1.6) 0.6(0.1) -
Vd=150 cm −4.8(-) - 0.8(0.3) -
Most errors occurred in the upper field. Indeed, downward distracters tended to yield more antisaccades than prosaccades: 3.75% of antisaccades against 0.42% of prosaccades, and 2.08% against 0.42% at 40 and 150 cm, respectively; the difference between the two distances failed to reach significance (Chi28,1 = 1.0, p = .317). The upward distracter at 40 cm did not yield antisaccades (in the lower visual field), while we observed 2.92% of prosaccades. No erratic saccade was detected for the upward distracter at 150 cm. 
These errors did not concern all the subjects. Four of the eight subjects showed prosaccades (range = 0.83–5%), and only three of them triggered spontaneous antisaccades (range = 0.83–7.50%). Timing and dynamic characteristics of vertical saccades (see Table 4) resembled those of horizontal saccades. In response to downward distracters, the scarce prosaccades had latencies below 300 ms and large amplitude (−5.3°), while spontaneous antisaccades showed latencies above 300 ms and small amplitudes (average of 0.7°). Prosaccades in response to upward distracter had a small amplitude, 1.8°. Notice, however, that it was larger than that of spontaneous antisaccades toward the down-ward distracter. 
To summarize, vertical distracters caused errors particularly at a close distance and when the distracter appeared in the lower field. The failure of suppression was expressed by frequent upward saccades, whatever the direction of the distracter, with slow regular latency and small amplitude. 
Overview
To compare the suppression capacity among the different locations in space, we added the rates of all errors (either pro- or anti-movements) for each distracter. The left-ward distracter at close (20 cm) was responsible for the highest error rate (11.67%), followed by the leftward distracter at 40 cm and the rightward distracter at 20 cm (both 5.83%). For vergence, it was convergence that induced most errors (9.17% for convergence from 40 to 20 cm; 5.52% for convergence from 150 to 20 cm). Finally, the downward distracter at close caused the highest error rate among the vertical distracters (4.17%). 
Failure of suppression measured by fixation instability
In this second analysis, we pooled all the position signals from our group of subjects after having excluded the movements reported above. We aimed at investigating whether the eyes slightly deviated from the distracter in either direction. 
Results are summarized in Figure 5. Group averages for both the distracter task and the no-distracter task are shown for each distracter. No global difference was found between the two tasks (Chi2 < 1) for lateral saccades in either direction (see Figure 5A–C), vertical saccades in either direction (see Figure 5F–G), and divergence (see Figure 5E). For divergence distracters, however, it is not excluded that divergent drift was present but lost due to the resolution of our infrared recording device. 
Figure 5
 
Averages of trajectories, after exclusion of movements shown in Figures 24, for the group of subjects in both the distracter task (full line) and the no-distracter task (dotted line). Group averages are shown separately for each type of distracter: distracter appearing laterally either leftward (left) or rightward (right) at viewing distances of 20 cm (A), 40 cm (B), or 150 cm (C); distracter calling for convergence (D) from 40 to 20 cm (left) or from 150 to 20 cm (right); distracter calling for divergence (E) from 40 to 150 cm (left) or from 20 to 150 cm (right); distracter appearing altitudinally either downward (left) or upward (right) at viewing distances of 40 cm (F) or of 150 cm (G). Trajectories are those of the saccadic horizontal signal for lateral saccades (A–C), of the vergence horizontal signal for vergence (D, E), and of the saccadic vertical signal for vertical saccades (F, G). Amplitude of movement in degrees is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to the onset of the distracter. The two vertical dotted lines delineate the gap period: the FP offset at time −200 ms and the D (distracter) onset at time 0 ms. N indicates the number of trials for the group of subjects for both the distracter task (full line) and the no-distracter task (dotted line). The Friedman statistics testing the global difference between the two tasks are reported in italics. NS = not significant. For convergence only, specific differences were found, starting at the point indicated by a double arrow.
Figure 5
 
Averages of trajectories, after exclusion of movements shown in Figures 24, for the group of subjects in both the distracter task (full line) and the no-distracter task (dotted line). Group averages are shown separately for each type of distracter: distracter appearing laterally either leftward (left) or rightward (right) at viewing distances of 20 cm (A), 40 cm (B), or 150 cm (C); distracter calling for convergence (D) from 40 to 20 cm (left) or from 150 to 20 cm (right); distracter calling for divergence (E) from 40 to 150 cm (left) or from 20 to 150 cm (right); distracter appearing altitudinally either downward (left) or upward (right) at viewing distances of 40 cm (F) or of 150 cm (G). Trajectories are those of the saccadic horizontal signal for lateral saccades (A–C), of the vergence horizontal signal for vergence (D, E), and of the saccadic vertical signal for vertical saccades (F, G). Amplitude of movement in degrees is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to the onset of the distracter. The two vertical dotted lines delineate the gap period: the FP offset at time −200 ms and the D (distracter) onset at time 0 ms. N indicates the number of trials for the group of subjects for both the distracter task (full line) and the no-distracter task (dotted line). The Friedman statistics testing the global difference between the two tasks are reported in italics. NS = not significant. For convergence only, specific differences were found, starting at the point indicated by a double arrow.
In contrast, a significant convergent drift was found in the distracter task for the distracters calling for convergence (see Figure 5D). When the FP was located at 40 cm and called for a convergence of 8.3° (see Figure 5D, left), the global difference between the distracter and the no-distracter tasks was significant (Chi28,48 = 115.3, p < .00001). 
A small convergent drift was initiated 136 ms after distracter onset and lasted 192 ms; the maximum amplitude was 0.21°. To perform specific comparisons, we first checked that the signal in the distracter task (i) did not differ from that of the no-distracter task and (ii) did not vary in amplitude, for the following periods: the fixation period (from −600 to −200 ms) and the gap period (from −200 to 0 ms). Then, each time interval of 20 ms within the test period (from 0 to +400 ms) was compared to the baseline fixation and the gap periods. The signal of the distracter task started to deviate significantly from that of the no-distracter task 200 ms after distracter onset (Z8 = 2.2, p = .025); the difference remained significant until the end of the time window. 
When the FP was located at 150 cm and called for a convergence of 14.7° (see Figure 5D, right), the global difference between the two tasks was also statistically significant (χ28,48 = 89.9, p = .00024). A small convergent drift started 126 ms after distracter onset, lasted 193 ms, and reached the amplitude of 0.12°, which was almost twice lower than that of convergence from 40 cm. Specific comparisons were similarly performed. The signal in the distracter task deviated significantly from that in the no-distracter task 220 ms after distracter onset (Z8 = 2.0, p = .049); again the difference between the two tasks remained significant until the end of the time window of interest. 
To summarize, convergence distracters were the most difficult to ignore. They yielded a convergent drift in the distracter task compared with the no-distracter task. This drift was initiated with a fast regular latency, and its amplitude tended to increase while the distance between the FP and the distracter decreased. 
Discussion
The main findings were the following: (1) The ability to ignore distracters was not perfect, leading to the generation of eye movements; (2) such errors were distributed unequally in 3D space-the spatial anisotropy consisted in difficulties to ignore distracters calling for convergence, and a tendency to make more errors in response to leftward and downward distracters; (3) distracters calling for saccade suppression yielded both pro- and antisaccades, with sub-populations of saccades different in nature; (4) for vergence, only distracters calling for convergence yielded errors that were always promovements; (5) and apart from erratic clear eye movements, a convergence drift was found for distracters calling for convergence. In the following sections, we move after methodological considerations to a discussion on the findings in terms of neurophysiological generation of eye movements, and a comment on spatial anisotropy of erratic eye movements. 
Methodological issues
In the present study, we used the upper limit of 500 ms for the inter-saccadic interval of SWJ. While a value of 200–300 ms is mentioned as the standard average of inter-saccadic interval of SWJ (Leigh & Zee, 1999), the standard upper limit is 400–500 ms. In their review, Elidan et al. (1984) reported that the upper limit for the inter-saccade delay in normal subjects varied from 400 to 500 ms, except in the study by Feldon and Langston (1977), who used an upper limit of 750 ms. Recently, Hafed and Clark (2002) also flagged as physiological SWJ pairs of opposing saccades with intervals up to 750 ms. Thus, our criterion was compatible with several reports in the literature. 
Another methodological issue that needs discussion is our 0.5° criterion to distinguish between fixational involuntary eye movements (particularly microsaccades) and eye movements induced by the task. In the literature, several thresholds have been used as the upper limit for spontaneous fixational microsaccades: 33 arcmin by Winterson and Collewijn (1976), 10 arcmin by Steinman, Haddad, Skavenski, and Wyman (1973), and 120 arcmin by Martinez-Conde, Macknik, and Hubel (2000). In their review, Martinez-Conde et al. (2004) reported upper thresh-olds for microsaccades ranging from 12 to 120 arcmin. But as mentioned by these authors, microsaccades cannot be defined on the basis of amplitude alone but should refer to any small involuntary saccades that occur during fixation. Hafed and Clark (2002) used an upper threshold of 1°, but found that 84% of their microsaccades were less than 0.5°; a second analysis including saccades with amplitude between 0.5 and 1° did not change the profile of their results. To conclude, we hypothesize that the majority of eye movements reported in the present study with amplitude between 0.5° and 2° were related to the distracter, without excluding the possibility that marginal items may represent the tail of a population of fixational spontaneous microsaccades. 
Neural substrate of inhibition
Oculomotor behavior alternates between periods of eye movements (saccade, pursuit, and vergence) and periods of fixation. Electrophysiological studies in animals, as well as lesion and brain-imaging studies in humans, allowed us to determine the neural substrate of eye movements for saccades, for pursuit, and less for vergence. Saccades are produced by a pulse step discharge of the extraocular motoneurons induced by a mechanism in the reticular formation of the brain stem involving excitatory and inhibitory burst neurons (for a review, see Scudder, Kaneko, & Fuchs, 2002). This saccade generator is innervated by the superior colliculus (SC) in the midbrain. The SC contains saccade-related neurons in the caudal pole of its intermediate layers (Moschovakis, Karabelas, & Highstein, 1988a, 1988b). At the cortical level, three main areas are involved in the triggering of saccades: the parietal eye fields (PEF), the frontal eye fields (FEF), and the supplementary eye fields (SEF) (for a review, see Pierrot-Deseilligny, Müri, Ploner, Gaymard, and Rivaud-Péchoux (2003b). 
The neural substrate of fixation is not so well under-stood. Eye fixation probably acts through inhibition of eye movements. Indeed, in parallel to the excitatory mechanisms mentioned above, a cascade of inhibitory mechanisms allows the modulation and blockage of saccades (Berthoz, 1996). At the brainstem level, burst neurons are under the inhibitory control of omnipause neurons (OPN) (Curthoys, Markham, & Furuya, 1984), which are them-selves directly activated by fixation neurons of the SC located in the rostral pole of its intermediate layers (Paré & Guitton, 1994). Saccade-related neurons of the SC are in-hibited by the fixation neurons of SC (Munoz & Wurtz, 1993a, 1993b), by the substantia nigra pars reticulata (Deniau & Chevalier, 1985; Hikosaka & Wurtz, 1983), and by the dorsolateral prefrontal cortex (DLPFC) through direct projections (Goldman & Nauta, 1976; Leichnetz, Spencer, Hardy, & Astruc, 1981). The substantia nigra itself is under the control of caudate neurons (Hikosaka, Sakamoto, & Miyashita, 1993) and a neural network involving the subthalamic nucleus (Matsumura, Kojima, Gardiner, & Hikosaka, 1992). 
A dysfunction at any level of this inhibitory cascade is responsible for the facilitation of unwanted saccades that may be different in nature depending on the affected structures: saccadic oscillations after dysfunction of OPNs (Ramat, Leigh, Zee, & Optican, 2005; Zee & Robinson, 1979), erratic saccades during fixation after a lesion of the SC (Pierrot-Deseilligny, Rosa, Masmoudi, Rivaud, & Gaymard, 1991), or reflexive erroneous saccades in the antisaccade task after lesions involving both the caudate nucleus (CN) and the substantia nigra (SN) in the Huntington’s disease, the CN, SN, and SC in the progressive supranuclear palsy, or after a focal lesion of either the DLPFC or the anterior cingulate cortex (see Introduction). 
The suppression or distracter task used in the present study offers the opportunity to create a conflict in the decision to move or to fixate, as the instruction calls for immobility of the eyes, whereas the stimulus calls for a movement. Such a task generates an imbalance between movement-related neurons and fixation-related neurons. This imbalance may even be enhanced by the use of a gap paradigm that involves a time interval between the extinction of the FP and the appearance of a target or distracter. In the gap paradigm, the latency of saccades is shortened by comparison with the simultaneous (no-gap) and the overlap paradigms, and some express saccades can occur (Fischer & Boch, 1983; Fischer & Ramsperger, 1984). For vergence along the median plane, latency is also shortened but no clear express vergence was reported (Coubard et al., 2004; Takagi et al., 1995; Tam & Ono, 1994). Express movements were found for vergence only when it was combined with a saccade (Coubard et al., 2004). The gap effect results from two components: a warning signal effect due to the offset of the FP (L. E. Ross & Ross, 1980; S. M. Ross & Ross, 1981) and a visual offset effect also called fixation release (Kingstone & Klein, 1993; Reuter-Lorenz, Hughes, & Fendrich, 1991). Electrophysiological studies in monkeys showed an increasing activity during the gap period and in association with the triggering of express saccades for a subset of saccade-related neurons in the SC (for a review, see Munoz, Dorris, Paré, & Everling, 2000) and in the FEF (Everling & Munoz, 2000). The reverse pattern-decreasing activity during the gap period and prior to an express saccade-was reported for fixation neurons in the prefrontal cortex (Brodman’s areas 8 and 46) of the monkey (Tinsley & Everling, 2002) but not in the SC (Dorris, Paré, & Munoz, 1997; Everling, Paré, Dorris, & Munoz, 1998). 
Our task caused 1.79% of erratic prosaccades in all, which was remarkably less than the rate of erratic prosaccades obtained in studies using the antisaccade task (e.g., 23 ± 17% in the study with 947 subjects by Evdokimidis et al., 2002, and Smyrnis et al., 2002). In addition, no express latency was found contrary to what is usually observed in the antisaccade task (Everling & Fischer, 1998; Munoz & Everling, 2004). These results suggest that the antisaccade task may be more complex than the suppression task. Distracters calling for saccades caused both prosaccades and antisaccades, whereas distracters calling for vergence caused provergence only. Taken together with the different latencies obtained for saccade on one hand (slow regular) and vergence on the other hand (fast regular), the results suggest that different inhibitory mechanisms may be involved in the two systems. The neural substrate of vergence, and a fortiori its inhibitory mechanisms, are less understood than those of saccade. At the brain stem level, there is anatomical and neurophysiological evidence for separate excitatory mechanisms of vergence and version (for a review, see Hung & Ciuffreda, 2002), but OPNs act as a gate for both conjugate and disconjugate movements (Mays & Gamlin, 1995). At the cortical level, the transcranial magnetic stimulation (TMS) over the right DLPFC was found to favor the triggering of reflexive contralateral saccades (Müri et al., 1999), whereas it did not influence the latency of convergence along the median plane; the latency of convergence was shortened by TMS over the right DLPFC only when the convergence was combined with a saccade (Coubard, Kapoula, Müri, & Rivaud-Péchoux, 2003). 
Spatial anisotropy of uninhibited eye movements
A left/right asymmetry was found in the errors. Subjects showed more difficulties to ignore a distracter located leftward than rightward, particularly at a close distance. For a leftward distracter at 20 cm, the errors were in the form of pro-saccades (6.67%) or spontaneous antisaccades (5%); at 40 cm, the errors were mostly spontaneous antisaccades (4.58%).These results are in line with the activation-orienting hypothesis by Kinsbourne (Kinsbourne, 1993; Reuter-Lorenz, Kinsbourne, and Moscovitch, 1990) according to which the distribution of attention in space is biased in the direction contralateral to the more activated hemisphere. Our suppression task was a basic visuo-spatial task, and we hypothesize that the right hemisphere was the more activated hemisphere consistently, with studies revealing its dominance in processing spatial information (Heilman, Bowers, Valenstein, & Watson, 1986; Posner, Petersen, Fox, & Raichle, 1988). Thus, spatial attention in our task was biased to the left direction, resulting in a higher rate of errors for leftward distracters. The fact that some errors were spontaneous antisaccades to the right is compatible with the physiological rightward bias in triggering saccades described in several studies (e.g., see Fischer & Weber, 1997). 
In the vertical plane, saccades tended to be triggered preferentially upward whatever the location of the distracter, in the lower or the upper field. Up-down asymmetry in the triggering of saccades consisting in shorter latencies for upward saccades was described by Goldring and Fischer (1997) and Pitzalis and Di Russo (2001). Faster triggering of upward saccades was confirmed by Zhou and King (2002), who demonstrated in addition, using a cued paradigm, a higher attentional sensitivity to upper targets, which could explain the up-down asymmetry observed in the generation of saccades. The higher attentional sensitivity described by Zhou and King may account for the tendency of our subjects to shift their gaze upward regardless of the direction of the distracter. Consistently, the mean amplitude of upward saccades tended to be higher (24% of distracter amplitude) when the distracter was in the upper field, than that of upward saccades in response to a distracter in the lower field (<10% of distracter eccentricity). 
The viewing distance influenced oculomotor responses for both lateral and vertical saccades. Sensory salience of the distracter (higher subtended visual angle at close than at far) may participate in the higher difficulty to ignore the distracters at close (either lateral calling for saccade or central calling for a convergence) than at far. But maintaining fixation at close also means sustaining convergence and requires more effort and/or attention than fixating at far. In line with this hypothesis, Yang et al. (2002) and Bucci et al. (2004) reported a shorter latency average for movements initiated from close (saccade and divergence) by comparison with movements initiated from far (saccade and convergence). For distracters calling for a convergence, we also observed that the ease to suppress was positively correlated to the distance separating the distracter from the fixation location. As the location of the convergence distracter was unchanged (20 cm), the proximity to the fovea of its image was stronger when fixating at 40 cm than when fixating at 150 cm. This result is consistent with the remote distracter effect showing that when two stimuli are presented simultaneously, the latency and metrics of the saccade are biased with a strength that is proportional with the proximity to the fovea (see Findlay & Walker, 1999). 
Conclusions
The ability of normal subjects to suppress eye movements to distracters presented at different locations was not perfect. We observed antisaccades even without any instructions asking to move, suggesting that, for saccades, the opposition behavior may be intrinsically linked to inhibition. Our distracter task constitutes a basic cognitive task, which may be useful to explore only inhibitory processes. It also gives the possibility to assess the directions and depths of 3D space for which inhibitory ability is more fragile. Such a task could be useful to study neuropsychiatric patients. 
Acknowledgments
The conception of the 3D suppression paradigm was provided by ZK. OC was funded by a fellowship of Neuro-Ophthalmology Berthe Fouassier, Fondation de France. Mechanics were completed by M. Ehrette, who was assisted by Y. Dupraz (LPPA), and electronics were completed by Pr G. Daunys (Siauliai University, Lithuania). The authors thank Pr. I. Evdokimidis for useful discussions. 
Commercial relationships: none. 
Corresponding authors: Olivier Coubard and Zoï Kapoula. 
Address: Laboratoire de Physiologie de la Perception et de l’Action, UMR7124 CNRS-Collège de France, 11 place Marcelin Berthelot, 75005 Paris, France. 
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Figure 1
 
(A). Condition 1 (left): Six light-emitting diodes (LEDs) were positioned on a table at eye level. The fixation point (FP) was the central LED at either 20 cm (close) or at 150 cm (far). When the close FP was lighted on, the distracter could be (1) either one of the two lateral LEDs at 20 cm (10° version) or (2) the central LED at 150 cm (14.7° divergence). When the FP was the central LED at150 cm, the distracter could be (1) either one of the two lateral LEDs at 150 cm (10° version) or (2) the center at 20 cm (14.7° convergence). Condition 2 (middle): Five LEDs were positioned on the same table. The FP was the central LED placed 40 cm away from the subject’s eyes. The distracter LED could be (1) either one of the two lateral LEDs at 40 cm (10° version) or (2) the center one at 20 cm (8.3° convergence) or the center one at 150 cm (6.4° divergence). Conditions 3 and 4 (right): Three LEDs were embedded in the vertical plane at a viewing distance of either 40 cm (condition 3) or 150 cm (condition 4). The FP was the central LED. The distracter LED could be one of the two altitudinal LEDs (7.5° version). (B). The gap paradigm was used for the distracter task. After a fixation period varying from 2 to 2.5 s, a temporal gap of 200 ms was introduced before the appearance of the distracter. The distracter was on for1.5 s, then a beep occurred indicating the 2-s pause (the subject was in a dark room). In the no-distracter task (control), the fixation period lasted 2–2.5 s. Then, the fixation LED was switched off and no distracter appeared. A beep occurred 1.7 s after the extinction of FP to indicate the pause of 2 s. Dotted rectangles indicate the time window of interest on which the analyses were restricted.
Figure 1
 
(A). Condition 1 (left): Six light-emitting diodes (LEDs) were positioned on a table at eye level. The fixation point (FP) was the central LED at either 20 cm (close) or at 150 cm (far). When the close FP was lighted on, the distracter could be (1) either one of the two lateral LEDs at 20 cm (10° version) or (2) the central LED at 150 cm (14.7° divergence). When the FP was the central LED at150 cm, the distracter could be (1) either one of the two lateral LEDs at 150 cm (10° version) or (2) the center at 20 cm (14.7° convergence). Condition 2 (middle): Five LEDs were positioned on the same table. The FP was the central LED placed 40 cm away from the subject’s eyes. The distracter LED could be (1) either one of the two lateral LEDs at 40 cm (10° version) or (2) the center one at 20 cm (8.3° convergence) or the center one at 150 cm (6.4° divergence). Conditions 3 and 4 (right): Three LEDs were embedded in the vertical plane at a viewing distance of either 40 cm (condition 3) or 150 cm (condition 4). The FP was the central LED. The distracter LED could be one of the two altitudinal LEDs (7.5° version). (B). The gap paradigm was used for the distracter task. After a fixation period varying from 2 to 2.5 s, a temporal gap of 200 ms was introduced before the appearance of the distracter. The distracter was on for1.5 s, then a beep occurred indicating the 2-s pause (the subject was in a dark room). In the no-distracter task (control), the fixation period lasted 2–2.5 s. Then, the fixation LED was switched off and no distracter appeared. A beep occurred 1.7 s after the extinction of FP to indicate the pause of 2 s. Dotted rectangles indicate the time window of interest on which the analyses were restricted.
Figure 2
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared laterally either leftward(left) or rightward (right) at viewing distances (Vd) of 20 cm (A), 40 cm (B), or 150 cm (C). Only saccades starting 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye horizontal signals): By convention, a positive deviation indicates a rightward movement, and a negative deviation indicates a leftward movement. The amplitude of movements (in degrees) is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to distracter onset. Gaze positions are relative and were offset at time −600 ms for clarity of display. For each distracter, the occurrence of prosaccades (Pro) and that of antisaccades (Anti) is indicated in bold. We report the averages and SDs of latency (ms), amplitude (°),and peak velocity (°/s) close to the corresponding trajectories. The two vertical dotted lines delineate the gap period: the FP offset at time \t-200 ms and the D (distracter) onset at time 0 ms.
Figure 2
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared laterally either leftward(left) or rightward (right) at viewing distances (Vd) of 20 cm (A), 40 cm (B), or 150 cm (C). Only saccades starting 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye horizontal signals): By convention, a positive deviation indicates a rightward movement, and a negative deviation indicates a leftward movement. The amplitude of movements (in degrees) is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to distracter onset. Gaze positions are relative and were offset at time −600 ms for clarity of display. For each distracter, the occurrence of prosaccades (Pro) and that of antisaccades (Anti) is indicated in bold. We report the averages and SDs of latency (ms), amplitude (°),and peak velocity (°/s) close to the corresponding trajectories. The two vertical dotted lines delineate the gap period: the FP offset at time \t-200 ms and the D (distracter) onset at time 0 ms.
Figure 3
 
Trajectories of pro- and antivergence observed in the distracter task only, when a distracter appeared in depth. The distracter LED could appear in front of the fixation LED, calling for a convergence from 40 to 20 cm (A) or from 150 to 20 cm (B). The distracter LED could appear behind the fixation LED, calling for a divergence from 40 to 150 cm (C) or from 20 to 150 cm (D). Only vergence starting 80 ms after distracter onset are shown. For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the vergence signal (difference between left eye and right eye horizontal signals) so that a convergence results in a positive deviation and a divergence in a negative one. Other notations as in Figure 2.
Figure 3
 
Trajectories of pro- and antivergence observed in the distracter task only, when a distracter appeared in depth. The distracter LED could appear in front of the fixation LED, calling for a convergence from 40 to 20 cm (A) or from 150 to 20 cm (B). The distracter LED could appear behind the fixation LED, calling for a divergence from 40 to 150 cm (C) or from 20 to 150 cm (D). Only vergence starting 80 ms after distracter onset are shown. For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the vergence signal (difference between left eye and right eye horizontal signals) so that a convergence results in a positive deviation and a divergence in a negative one. Other notations as in Figure 2.
Figure 4
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared altitudinally either downward (left) or upward (right) at viewing distances (Vd) of 40 cm (A) or 150 cm (B). Only the saccades triggered at least 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye vertical signals): A positive deviation indicates an upward movement and a negative deviation indicates a downward movement. No pro- or antisaccades were observed for the upward distracter at 150 cm. Other notations as in Figure 2.
Figure 4
 
Trajectories of pro- and antisaccades observed in the distracter task only, when a distracter appeared altitudinally either downward (left) or upward (right) at viewing distances (Vd) of 40 cm (A) or 150 cm (B). Only the saccades triggered at least 80 ms after distracter onset are shown (even though a drift may be visible before). For each type of movement, we show all instances of records for the group of subjects. Trajectories are those of the saccadic signal (average of left eye and right eye vertical signals): A positive deviation indicates an upward movement and a negative deviation indicates a downward movement. No pro- or antisaccades were observed for the upward distracter at 150 cm. Other notations as in Figure 2.
Figure 5
 
Averages of trajectories, after exclusion of movements shown in Figures 24, for the group of subjects in both the distracter task (full line) and the no-distracter task (dotted line). Group averages are shown separately for each type of distracter: distracter appearing laterally either leftward (left) or rightward (right) at viewing distances of 20 cm (A), 40 cm (B), or 150 cm (C); distracter calling for convergence (D) from 40 to 20 cm (left) or from 150 to 20 cm (right); distracter calling for divergence (E) from 40 to 150 cm (left) or from 20 to 150 cm (right); distracter appearing altitudinally either downward (left) or upward (right) at viewing distances of 40 cm (F) or of 150 cm (G). Trajectories are those of the saccadic horizontal signal for lateral saccades (A–C), of the vergence horizontal signal for vergence (D, E), and of the saccadic vertical signal for vertical saccades (F, G). Amplitude of movement in degrees is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to the onset of the distracter. The two vertical dotted lines delineate the gap period: the FP offset at time −200 ms and the D (distracter) onset at time 0 ms. N indicates the number of trials for the group of subjects for both the distracter task (full line) and the no-distracter task (dotted line). The Friedman statistics testing the global difference between the two tasks are reported in italics. NS = not significant. For convergence only, specific differences were found, starting at the point indicated by a double arrow.
Figure 5
 
Averages of trajectories, after exclusion of movements shown in Figures 24, for the group of subjects in both the distracter task (full line) and the no-distracter task (dotted line). Group averages are shown separately for each type of distracter: distracter appearing laterally either leftward (left) or rightward (right) at viewing distances of 20 cm (A), 40 cm (B), or 150 cm (C); distracter calling for convergence (D) from 40 to 20 cm (left) or from 150 to 20 cm (right); distracter calling for divergence (E) from 40 to 150 cm (left) or from 20 to 150 cm (right); distracter appearing altitudinally either downward (left) or upward (right) at viewing distances of 40 cm (F) or of 150 cm (G). Trajectories are those of the saccadic horizontal signal for lateral saccades (A–C), of the vergence horizontal signal for vergence (D, E), and of the saccadic vertical signal for vertical saccades (F, G). Amplitude of movement in degrees is plotted as a function of time (in ms) within the window of interest starting from −600 ms and ending +400 ms relative to the onset of the distracter. The two vertical dotted lines delineate the gap period: the FP offset at time −200 ms and the D (distracter) onset at time 0 ms. N indicates the number of trials for the group of subjects for both the distracter task (full line) and the no-distracter task (dotted line). The Friedman statistics testing the global difference between the two tasks are reported in italics. NS = not significant. For convergence only, specific differences were found, starting at the point indicated by a double arrow.
Table 1
 
Design. N indicates the number of trials within a block. FP = fixation point.
Table 1
 
Design. N indicates the number of trials within a block. FP = fixation point.
Distracter Task No Distracter Task (control)
Nb of distracters (one at a time) Nb of blocks Nb of FP (one at a time) Nb of blocks
Condition 1 (horizontal) 6 3 (N = 60) 2 1 (N = 60)
Condition 2 (horizontal) 4 2 (N = 60) 1 1 (N = 30)
Condition 3 (vertical) 2 1 (N = 60) 1 1 (N = 30)
Condition 4 (vertical) 2 1 (N = 60) 1 1 (N = 30)
Total = 7 Total = 4
Table 2
 
Parameters of lateral erratic saccades. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the left/right asymmetry (L/R), and for the viewing distance (20/40/150). p < .05; ns = no significant difference.
Table 2
 
Parameters of lateral erratic saccades. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the left/right asymmetry (L/R), and for the viewing distance (20/40/150). p < .05; ns = no significant difference.
Prosaccades (2.64%) Antisaccades (2.64%) All
Frequency (%) Left Right L/R Left Right L/R
Vd=20 cm 6.67 2.50 ns 5.00 3.33 ns 4.37
Vd=40 cm 1.25 2.08 ns 4.58 0.42 * 2.08
Vd=150 cm 1.25 2.08 ns 1.67 0.83 ns 1.45
20/40/150 > ns ns ns ns *
Latency (ms)
Vd=20 cm 292(50) 249(81) 314(38) 313(41)
Vd=40 cm 264(46) 196(126) 305(54) 85(-)
Vd=150 cm 293(46) 272(39) 292(93) 343(19)
Amplitude (°)
Vd=20 cm −4.6(4.2) 4.1(4.1) 1.2(0.5) −1.1(0.4)
Vd=40 cm −6.7(4.9) 1.6(1.1) 1.2(0.5) −0.6(−)
Vd=150 cm −10.1(0.3) 7.5(3.8) 1.0(0.1) −1.1(0.4)
Table 3
 
Parameters of erratic vergence. FP at 150/20 cm: fixation point at 150 cm for convergence and 20 cm for divergence. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the convergence/divergence asymmetry (C/D) and for the viewing distance (40/150). *p < .05; ns = no significant difference.
Table 3
 
Parameters of erratic vergence. FP at 150/20 cm: fixation point at 150 cm for convergence and 20 cm for divergence. For latency and amplitude, we provide the average and the SD in parentheses. Statistics on frequencies only, for the convergence/divergence asymmetry (C/D) and for the viewing distance (40/150). *p < .05; ns = no significant difference.
Provergence (3.75%) Antivergence (0.62%) All
Frequency (%) Convergence Divergence C/D Convergence Divergence C/D
FP at 40 cm 8.75 0.42 * 0.42 1.25 ns 2.71
FP at 150/20 cm 5.42 0.42 ns 0 0.83 ns 1.67
40/150 > ns ns ns ns ns
Latency (ms)
FP at 40 cm 152(18) 132(−) 125(−) 170(54)
FP at 150/20 cm 164(49) 83(−) 88(6)
Amplitude (°)
FP at 40 cm 1.9(2.4) −0.7(−) −0.6(−) 0.8(0.1)
FP at 150/20 cm 3.8(6.3) −0.7(−) 0.8(0.3)
Table 4
 
Parameters of erratic vertical saccades. For latency and amplitude, we provide the average and the SDs in parentheses. Statistics are on frequencies only for the down/up asymmetry (D/U) and for the viewing distance (40/150). ns = no significant difference.
Table 4
 
Parameters of erratic vertical saccades. For latency and amplitude, we provide the average and the SDs in parentheses. Statistics are on frequencies only for the down/up asymmetry (D/U) and for the viewing distance (40/150). ns = no significant difference.
Prosaccades (0.94%) Antisaccades (1.45%) All
Frequency (%) Down Up D/U Down Up D/U
Vd=40 cm 0.42 2.92 ns 3.75 0 ns 1.77
Vd=150 cm 0.42 0 ns 2.08 0 ns 0.62
40/150 > ns ns ns ns ns
Latency (ms)
Vd=40 cm 249(-) 295(91) 282(39) -
Vd=150 cm 247(-) - 297(34) -
Amplitude (°)
Vd=40 cm −5.9(-) 1.8(1.6) 0.6(0.1) -
Vd=150 cm −4.8(-) - 0.8(0.3) -
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