Running head: INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
Inhibition of Return Across Eye and Object Movements: The Role of Prediction
Hannah M. Krüger and Amelia R. Hunt
University of Aberdeen, UK
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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Abstract
Responses are slower to targets appearing in recently-inspected locations, an effect known as
Inhibition of Return (IOR). IOR is typically viewed as the consequence of an involuntary
mechanism that prevents re-inspection of previously visited locations and thereby biases
attention towards novel locations during visual search. For an inhibitory tagging mechanism to
serve this function effectively, it should be robust against eye movements and the movements of
objects in the environment. We investigated whether the predictability of motion supports the
coding of inhibitory tags in spatiotopic coordinates across eye movements and object-based
coordinates across object motion. IOR was observed in both retinotopic and spatiotopic
coordinates across eye movements, regardless of the predictability of the eye movement
direction. In a matching experiment, but with predictable or unpredictable object motion instead
of eye movements, IOR was reduced in magnitude by object motion and was not observed in
object-based coordinates, even when the motion was predictable. Together the results suggest
inhibitory tags can track objects as they move across the retina, but only when this motion is selfgenerated. We conclude that efference copy, not prediction, plays a key role in maintaining
inhibition on previously-attended objects across saccades.
Keywords: Inhibition of Return, inhibitory tagging, visual attention, eye movements
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Responses to targets appearing in the same location as an uninformative cue tend to be
faster than in other locations (Posner, 1980), but only when the duration between the cue and
target is short. When targets appear more than 200-300ms after the cue, responses to targets in
the cued location are slower than the uncued location (Posner & Cohen, 1984). This delay in
target detection at longer cue-target intervals is called Inhibition of Return (IOR). IOR is a robust
effect that has been reproduced hundreds of times since the seminal study by Posner and Cohen
in 1984. Posner and Cohen originally postulated that IOR reflects an attentional orienting bias.
That is, the exogenous cue attracts attention reflexively, and if the target appears just briefly after
the cue, attention is still in place and therefore facilitates a response. Over time, however,
attention retreats from the cued location and this location is then inhibited in favour of new
locations.
In line with the assumption that IOR indexes inhibitory tags that orient attention towards
novelty, Klein (1988) proposed that inhibitory tagging can facilitate visual search. One study that
has delivered strong support for such a claim is that of Klein and MacInnes (1999), who recorded
eye movements while participants searched for “Waldo” (a character in a red-striped shirt and
glasses) in a cluttered “Where’s Waldo”TM scene. Participants were also instructed to move their
eyes as quickly as possible to any probes (black disks) appearing on the display. These probes
could appear at the previously fixated location, at the penultimate fixation, or in control locations
that had not yet been fixated. Saccades back to previously fixated locations were slower than
saccades to locations 180 degrees away from the previous fixation, and this result has been
reproduced by others (Dodd, van Stigchel, & Hollingworth, 2009; MacInnes & Klein, 2003;
Smith & Henderson, 2009; 2011). This is evidence that IOR is observed in a visual search
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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context, consistent with the interpretation that it reflects inhibitory tags that bias attention
towards novel locations during visual search.
The Reference Frame of IOR
For an inhibitory tagging mechanism to efficiently facilitate foraging, it must be coded in
spatiotopic (i.e., environmental or object- based) coordinates. If instead it were coded in
retinotopic (i.e., gaze-centred) coordinates, inhibitory tags would shift spatially with the eye
movements and would impede search in unexplored locations. Supporting a spatiotopic reference
frame for IOR, the aforementioned studies investigating IOR in a visual search context have
found IOR not only in the previously fixated location, but also in the location fixated two
saccades previously (the 2-back location). This supports the idea that IOR indexes an attentionrelated phenomenon that is coded in spatiotopic locations, rather than reflecting either a change
in sensitivity to a location on the retina, or a motor bias, such as an inhibited saccade vector or a
location on the retina.
IOR has also been observed in spatiotopic coordinates in cue-target experiments (Abrams
& Pratt, 2000; Maylor & Hockey, 1985; Posner & Cohen, 1984; van Koningsbruggen, Gabay,
Sapir, Henik & Rafal, 2009). For example, Posner and Cohen (1984) investigated the reference
frame of IOR by cueing a location and then instructing observers to make eye movements to a
series of three locations. Subsequently, a target appeared at either the retinotopic or the
spatiotopic location of the cue. Participants were slower to respond to targets appearing in the
cued spatiotopic coordinates than to targets in the cued retinotopic location. However, more
recent evidence suggests that IOR is coded in both frames of reference. For example, Pertzov,
Zohary, and Avidan (2010), using saccades to peripheral targets as a response, find that IOR is
coded in spatiotopic coordinates just briefly after an eye movement, especially for cued targets
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that appear in the same hemifield as the cue. Nonetheless, they also observed a retinotopic
inhibition. Similarly, Hilchey, Klein, Satel and Wang (2012) and Mathot and Theeuwes (2010)
report both spatiotopic and retinotopic IOR across eye movements for saccadic responses to
targets and Sapir, Hayes, Henik, Danziger, and Rafal (2004) have shown a similar pattern for
manual responses to targets. Abrams and Pratt have shown that IOR is spatiotopic with manual
responses to a peripheral probe target, but IOR is retinotopic for saccadic responses to a central
arrow target. Together these studies suggest that IOR can be observed in both the spatiotopic and
retinotopic locations of cues, and that the factors that determine in which reference frame IOR
will be more robust are not yet fully understood.
A similar question to that about the reference frame of IOR concerns whether IOR is
object-based or location-based. To bias attention away from previously-inspected objects, which
can vary in size and can change location on the retina, inhibitory tagging would need to be
applied not to a limited and static location on the retina, but to whole objects. There is substantial
evidence from static displays that whole objects are inhibited (Chou & Yeh, 2008; Jordan &
Tipper, 1998; Leek, Reppa, & Tipper, 2003). Jordan and Tipper (1998), for example, illustrate
that if apparent objects (Kanisza squares) were cued, IOR was larger in magnitude than if a cue
appeared in a similar location but without apparent objects. Furthermore, Tipper, Driver and
Weaver (1991) showed that when an object is cued and subsequently moved, responses to targets
appearing in the cued object are slower even though the object occupies a new location in space.
It was also found that responses to targets appearing in the previous location of the moved object
were slower than uncued locations, suggesting inhibitory tags are both object-based and locationbased (Tipper, Weaver, Jerreat, & Burak, 1994). These findings have been challenged by Müller
and von Mühlenen (1996), who conducted a study with seven experiments in all of which IOR
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was largely location-based rather than object-based. Indeed, cued objects were facilitated, rather
than inhibited, when cued objects followed common motion patterns, for example, from left to
right (as in reading) or from top to bottom (falling with gravity). Thus, similar to the conclusions
made about the reference frame of IOR across eye movements, it appears as though IOR can be
applied to cued, moving objects, but this inhibition is not always applied. What circumstances
lead to robust object-based IOR is an open question.
Both spatiotopic IOR and object-based IOR are assumed to reflect an inhibitory tag that
disengages from the retinotopic location of the cue, and moves with objects as they move on the
retina. Given these similarities between them, it seems plausible that spatiotopic and objectbased IOR could reflect the same general mechanism. Indeed, if inhibitory tags were entirely
object-based then they would, by definition, also be spatiotopic. However, they also differ, in that
when the eyes move, the motion of objects on the retina is produced internally by the observer.
This motion is therefore expected and predictable. In the case of object-based IOR, the motion of
the object is generated externally, and cannot be predicted with certainty.
The ability to predict the upcoming motion with certainty may play an important role in
whether inhibitory tags are preserved on objects that move on the retina. However, it is also
possible that there is something special about retinal motion that is generated by an eye
movement, over and above its predictability. Indeed, recently it has been suggested that
spatiotopic IOR may be supported by a saccade-specific mechanism known as predictive
remapping (Abrams & Pratt, 2000; Mathôt & Theeuwes, 2010; Pertzov et al., 2010; van
Koningsbruggen et al., 2009). Visual cells in several brain areas, including lateral interparietal
cortex (LIP) and frontal eye fields (FEF) have been shown to respond to visual stimuli shortly
before an executed eye movement even though these stimuli will only fall into their receptive
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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field after the completion of this eye movement (Duhamel, Colby, & Goldberg, 1996).
Remapping has been linked to signals coming from superior colliculus (SC), a midbrain structure
associated with eye movement control, suggesting remapping is based on a copy of the efferent
saccadic motor command (Sommer & Wurtz, 2002; 2006). In other words, cells in some visual
areas of the brain use information about upcoming eye movements to prepare for expected
changes in the retinotopic map. The same mechanism may support spatiotopic inhibitory tagging
across saccades. Maintaining inhibitory tags on moving objects, however, cannot rely on exactly
the same mechanism, because the changes on the retina are not self-generated and therefore lack
an important aspect of predictive remapping: the efference copy. If object-based IOR differs from
spatiotopic IOR even when object motion is perfectly predictable, it would suggest that efference
copy plays an important role in maintaining inhibitory tags across saccades.
We therefore examined whether a general prediction-based mechanism could explain
both spatiotopic IOR across eye movements and object-based IOR across object motion. We
manipulated predictability by either blocking the direction of motion (predictable) or randomly
interleaving it within each block (unpredictable). We first examined the role of predictability in
maintaining IOR across saccades. In Experiment 1a we tested IOR across eye movements when
the direction of the eye movement was blocked and therefore predictable. In Experiment 1b we
also tested IOR across eye movements but the direction of the eye movement was mixed and
therefore unpredictable. If spatiotopic inhibitory tags rely on saccadic remapping alone then IOR
should be spatiotopic to a similar extent under these two conditions. Alternatively, the inhibition
of attended objects in their post-saccadic coordinates may depend to some extent on
foreknowledge about where these objects will appear on the retina in the future, in which case
the predictability of future eye movement directions may facilitate spatiotopic IOR.
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
In Experiment 2 we investigated location-based and object-based IOR by moving the
objects externally across the retina in a manner that mimicked the saccadic displacement of
Experiment 1. Again we manipulated predictability across object displacement, by running a
predictable and an unpredictable displacement condition. If predictability of object motion is a
crucial factor in object-based IOR then IOR should be object-based with predictable motion but
remain location-based with unpredictable motion.
Experiment 1a: Saccades with the direction blocked
Method
Participants
Twenty-eight participants (19 female, average age 22.25) participated in this study. All
participants had normal or corrected to normal vision. Some participants participated for course
credit (11), the rest volunteered.
Apparatus
An Eyelink 1000 (SR Research, Mississauga, Canada) was used for video based eye
tracking with a sample rate of 1000Hz. Only the right eye was monitored. The camera was
placed in the desktop mount, with a chin and forehead rest at a viewing distance of 50cm, in
front of an 85Hz 17inch CRT monitor with a resolution of 1024x768. The experiment was
programmed and run using Experiment Builder (SR Research) on a Macintosh Pro running
Windows XP.
Stimuli and procedure
Throughout this experiment and the following ones, the participant's primary task was to
perform a manual detection, that is, to press a specified button on a game controller as soon as
8
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the target stimulus (+) appeared anywhere on the screen. Participants were instructed to hold the
game controller with both hands and use the right thumb to press the button.
Each experiment and subsequently each block started with a nine-point calibration
sequence. In some cases the nine-point calibration was substituted with a five-point calibration
(only for participants with corrected vision). Each trial began with a drift correction: Participants
were instructed to fixate a dot in the middle of a blank screen and press a specified button with
their left thumb. If fixation was stable the trial would begin. Four boxes (outlined squares) 1.3˚ in
size were presented at each corner of an invisible square, 3.4˚ in length/height (see Figure 1). The
background was white. The top left and bottom right boxes were green [0, 150, 0] and the top
right and bottom left boxes were red [250, 0, 0]. These boxes were surrounded by a larger black
square, 15.6˚ in length/height1. All objects remained in this position throughout the experiment
and there were three fixation dots spread evenly across the horizontal midline between the upper
and lower two boxes all 3.4˚ apart from each other. After 500 ms the cue appeared: One of the
boxes filled with light grey [200,200,200] for 50ms. At 750ms into the trial (200ms after cue
offset) an auditory signal (female voice) said “stay” indicating that fixation was to be maintained
on the fixation dot straight ahead. At 1550ms (1050ms after the cue) the target ‘+’ (0.6 degrees)
appeared in one of the four boxes and remained visible for 500ms. The cue and target were
equally likely to appear in any of the four locations. Ten percent of all trials were catch trials
where no target appeared.
In Experiment 2, when object motion is introduced, the motion could be seen as either a shift of
all four boxes shifting together, or as two boxes jumping from one side to the other (as in the
Ternus illusion). The uniquely coloured boxes and a surrounding larger square force the
interpretation of four boxes shifting together. For consistency across the experiments this same
display was used in Experiment 1.
1
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In motion trials the same voice said “right” or “left”, indicating that an eye movement to
the fixation dot to the right or left of the central fixation dot should be made. The trial ended with
the button press or 2750ms after trial onset. After each correct response a positive feedback
sound was released. For each incorrect response (responding on catch trials, pressing the wrong
button, or not pressing the response button within the given time-interval) a negative feedback
sound was released. Each condition (stay, left, right) started with 12 training trials and consisted
of 4 blocks with 36 trials in each block. Left and right conditions were collapsed and treated as
one motion condition. The order of the conditions was counterbalanced so that the no motion
condition occurred equally often as the first, second, and third block.
>INSERT FIGURE 1 AROUND HERE <
Targets were classified as 1) cued targets on no saccade trials; 2) targets appearing on the
same retinotopic location as the cue (on motion trials) or 3) targets appearing in the cued
spatiotopic location (on motion trials). As uncued control locations for each of these categories,
we used the opposite box in the same column (for example, if the cued location is the upper left
square, the uncued location would be the lower-left square, and vice versa). We chose to compare
the cued location to its respective mirror uncued location (rather than comparing it to all other
uncued locations) as this led to an equal number of trials within each pair of cued and uncued
conditions and controlled for distance and direction relative to fixation. Trials falling into the
above categories comprised ~60% of trials. The remaining trials were catch trials (11% of all
trials) and trials where the cues and targets did not form any of the pairs described above (50% of
no motion trials and 25% of motion trials).
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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Results and Discussion
Trials were excluded from analysis if an eye movement was detected that moved further
than 1.3° away from the saccade target (5.0%). Trials with manual reaction times faster than
150ms or slower than 1000ms were also excluded (2.2%). Saccades landed on the target
accurately, although small under- and overshoots followed by corrective saccades were common
(37.5%). As long as the second fixation was acquired, we included these trials in the analysis
because remapping has been shown to be based on the intended, rather than the actual, saccade
target (e.g. Bahcall & Kowler, 1999). The saccade-to-target interval (STI) was taken as the
duration from the end of the saccade to the onset of the target. In the case of corrected saccades,
we used the end time for the saccade that landed on the second fixation. Trials were excluded if
STI was greater than 700ms or less than 180ms (17.4%)2. Subjects having less than 50% of trials
(i.e. 15 observations) remaining after exclusions in any of the defined target type conditions, or
those who pressed the button on more than 15% of catch trials (on average 5.8% erroneous
responses were recorded after exclusion) were excluded. On this basis three subjects were
excluded. Mean STI, saccadic latency and saccade to target onset asynchrony (STOA) are
displayed in Table 1.
>INSERT FIGURE 2 AND TABLE 1 AND TABLE 2 AROUND HERE <
The results are shown in Figure 2 and Table 2. A 3x2 repeated measures ANOVA with
Target Type (no saccade, retinotopic and spatiotopic) and Cueing (cued and uncued) revealed a
significant main effect of Cueing, F (1, 24) = 21.612; p < .001; ηp2= .474. The main effect of
2
We decided to drop trials with an STI smaller than 180ms or larger than 700ms to make STI in experiments 1a and
1b more comparable. Target onsets were not time-locked to the end of the eye movements and due to the predictable
direction in E1a, STIs were larger than in E1b. Additionally, dropping the extreme STI values in the eye movement
experiments made the timing of the retinal motion relative to the target onset time in these two experiments more
comparable to Experiment 2.
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Target Type (F (2, 48) = 1.289; p = .286) and the interaction (F < 1) were not significant,
indicating that IOR was present to a similar extent, regardless of the Target Type3.
IOR was observed in both spatiotopic and retinotopic coordinates across eye movements,
consistent with three recent studies (Hilchey et al., 2012; Mathot & Theeuwes, 2010; Pertzov et
al., 2010). It is important to note that these three studies used saccadic responses, while we used
manual responses. IOR was previously suggested to be more strongly spatiotopic for manual
responses and more strongly retinotopic for saccadic responses (Abrams & Pratt, 2000), so we
might have expected to produce predominantly spatiotopic IOR in our experiment. However,
Sapir et al. (2004) also observed both retinotopic and spatiotopic IOR for manual responses,
consistent with our current results. Unlike previous studies, our design also allowed us to directly
compare the retinotopic and spatiotopic IOR effect to IOR in a no-eye movement baseline
condition. We found no evidence of a significant reduction in the overall magnitude of IOR when
the eyes move.
In Experiment 1b we randomly interleave the trials of Experiment 1a, so that the
directions are mixed and unpredictable at the onset of the cue. If predictability of the saccade
direction is an important factor in maintaining inhibitory tags in spatiotopic coordinates, this
experiment should produce weaker spatiotopic IOR.
Experiment 1b: Saccades in mixed directions
Method
Participants
3
Unlike Pertzov et al., we did not observe a larger spatiotopic effect when the cue and target appear in the same
hemifield. However, there were a number of differences between their experiment and ours that could explain the
discrepancy, including response modality and the timing of the target onset relative to the saccade.
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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Thirty-one participants (20 female, average age 21.9) participated in this study. All
participants had normal or corrected to normal vision. Some participants participated for course
credit (10), others volunteered.
Apparatus, stimulus and procedure
Apparatus, stimuli and procedure were the same as in Experiment 1a, with the following
exceptions. First, the three different conditions of the separated blocks from Experiment 1a were
here randomly interleaved within each block. Second, the word “straight” was used in place of
the word “stay” to instruct subjects to maintain fixation on the no saccade trials. Third, the
Eyelink 1000 tower mount was used instead of the desktop mount. Fourth, if any eye movements
deviated further than 2° away from the horizontal midline (and towards any of the four object
markers), an error message was displayed and the trials were recycled (7.4% of trials had to be
repeated, but 28.2% of these were due to blinks). The experiment started with 12 practice trials
followed by 8 blocks of 54 trials, between which participants could rest.
Results and Discussion
Trials were excluded from analysis if an eye movement was made in the wrong direction
(7.2%), if responses were faster than 150ms or slower than 1000ms (3.5%), or if the wrong
button was pressed (1.1%). Trials were also excluded if STI was larger than 700ms or smaller
than 180ms (30.5%). Subjects with less than 50% of trials (i.e. 15 observations) in any of the
defined target types or with more than 15% responses on catch trials were excluded from the
analysis. On this basis nine participants were excluded. The average response rate on catch trials
after exclusion was 8.0%. As in Experiment 1a, small corrective saccades were relatively
common (22.1%) and trials where they occurred were not excluded. The mean STI was
317.12ms (SEM 5.32), and detailed saccade information can be found in Table 1.
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The results are shown in Figure 2 and Table 2. The same analysis as for Experiment 1a
revealed a main effect of Cueing, F (1, 21) = 11.081; p < .005; ηp2 = .345. The main effect of
Target Type (F (2, 42) = 1.082; p = .348) and the interaction of Cueing and Target Type (F < 1)
were not significant.
Direct comparison of Experiment 1a and 1b. The pattern of Experiment 1b looks very
similar to Experiment 1a. To statistically evaluate whether the two experiments produced
different results, we directly compared Experiment 1a and Experiment 1b in A 2x3x2 ANOVA
with Cueing (cued, uncued) and Target Type (no saccade, spatiotopic and retinotopic) as withinsubjects factors and with Experiment (Experiment 1a and 1b) as a between-subjects factor. The
analysis revealed a main effect of Cueing, F (1, 45) = 31.597; p < .001; ηp2 = .418, again
indicating the presence of IOR. The main effect of Target Type was not significant (F < 1). The
between-subjects factor Experiment was significant, F (1, 45) = 5.253; p < .05; ηp2 = 105,
reflecting slower RTs in Experiment 1a (predictable eye movement direction). None of the
interactions were significant (Target Type and Experiment, F (2, 90) = 1.720; p > .05; Cueing
and Experiment, F (1, 45) = 1.200; p > .05; Target Type and Cueing, F < 1), including the threeway interaction (F < 1), indicating that the predictability of eye movement direction had no
significant effect on the magnitude of IOR or its spatial distribution.
In summary, these findings indicate that IOR can be maintained across a saccade, and that
it occurs in both spatiotopic and retinotopic frames of reference. Furthermore, spatiotopic IOR is
not dependent on, or strengthened by, the ability to reliably predict the direction of an upcoming
eye movement. These results together suggest efference copy could play a key role in
maintaining inhibitory tags across changes in retinal position caused by saccades. Experiment 2
tests the role of efference copy by examining whether IOR can be maintained across similarly-
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
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sized shifts in an object’s retinal location, but when the shifts are produced not by the
participant’s own eye movements, but by external object motion. We examined both predictable
and unpredictable object motion.
Experiment 2: Object Shifts
Method
Participants
Twenty-four participants (15 female, mean age 24.6 years) participated in this study.
Participants volunteered (10) or were reimbursed £10 for their time. All participants were
recruited through the University of Aberdeen and had normal or corrected to normal vision.
Apparatus, stimulus and procedure
The stimuli and procedure were the same as Experiment 1a with the following
exceptions. There was only one fixation dot in the centre of the screen. Participants were
instructed to fixate this fixation dot throughout the trial. In motion trials, the four boxes and the
larger surrounding box shifted 3.4° to the left or to the right, 550ms after cue onset (the shift is
roughly equal to the average saccade end-time of Experiment 1). This shift resulted in, for
example, the left two boxes replacing the right two boxes and the right boxes shifting further into
the periphery (and the other way around for a shift to the left). See Figure 3 for reference. In no
motion trials, the objects remained in the same position throughout the trial.
>INSERT FIGURE 3 AROUND HERE <
All participants completed a blocked and a mixed condition. During the blocked
condition, the objects would either not shift (72 plus 12 practice trials) or would shift to the right
(72 plus 12 practice trials) or to the left (72 plus 12 practice trials) on all trials within a block.
During the mixed condition the shifts of the objects was randomly interleaved such that on a
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given trial they could shift to the left, shift to the right, or remain in their initial position (216
plus 12 practice trials). There was a break after every 36 trials throughout the different
conditions. To counterbalance, each of the 24 possible orders of these four sets (no motion, left,
right, and mixed) was completed by one subject. Subjects attended two experimental sessions
and performed all four blocks in each one of them, so the total number of trials in the experiment
was 864, not including practice. The sessions lasted 45-60 minutes and there was a minimum
delay of four hours and a maximum delay of four days between the first and the second session.
Targets were classified in a similar manner as in Experiment 1a and 1b. However,
retinotopic targets are now referred to as location-based because they occupy the same location
in space and the same location on the retina across object displacement, but are associated with a
different object. Object-based targets, similar to spatiotopic targets in Experiment 1, appear on
the same object as the previous cue, but after the object has shifted to a different location on the
retina.
Results and Discussion
Trials were excluded from analysis if an eye movement larger than 1.3° away from
fixation was detected (5.3%), or if manual reaction time was faster than 150ms or slower than
1000ms (3.3%). Subjects were excluded from analysis if they had less than 50% of trials (i.e. 15
observations) remaining in any one target type condition after these criteria were applied, or if
they responded to more than 15% of catch trials. On this basis three participants were excluded.
After exclusions, responses were made on 5.1% of catch trials. The results are shown in Figure 2
and Table 3. For simplicity, and to mirror the analyses in Experiment 1a and 1b, we first
examined blocked and mixed sessions separately.
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>INSERT TABLE 2 AROUND HERE<
Blocked session. We ran a 2x3 repeated-measures ANOVA with Cueing (cued or uncued)
and Target Type (no motion, location-based and object-based) as factors. The main effect of
Cueing was significant, F (1, 20) = 11.462; p < .005; ηp2 = .364, reflecting the presence of IOR.
The main effect of Target Type was also significant, F (3, 60) = 17.608; p < .001; ηp2 = .468, as
motion trials had faster RTs than no motion trials. Lastly, Cueing and Target Type qualified for an
interaction, F (2, 40) = 4.854; p <.05; ηp2 = .195. Planned comparison confirmed that IOR was
present only in no motion trials (t (20) = 4.138; p < .001), and not in any of the motion
conditions (ts < 1).
Mixed session. The same ANOVA conducted on the mixed session revealed a significant
effect of Cueing, F (1, 20) = 8.245; p < .001; ηp2 = .292. The main effect of Target Type was also
significant, F (2, 40) = 195.940; p < .001; ηp2 = .907, reflecting slower RTs on no motion trials
than motion trials. The interaction of Cueing and Target Type was also significant, F (2, 40) =
5.504; p < .01; ηp2 = .216, indicating that IOR was present in some Target Types but not in
others. Planned comparison revealed that this interaction occurred because there was significant
IOR in the no motion condition (t (20) = 2.744; p < .05) and in location-based coordinates (t (20)
= 2.33; p < .05); but not object-based coordinates (t (20) = 1.716, p > .05; with cued targets
having numerically faster RTs).
Direct Comparison of blocked and mixed conditions. To evaluate whether predictability
of object motion had an effect on the allocation of IOR, we conducted a 2x3x2 ANOVA with
Cueing (cued and uncued), Target Type (no motion, location-based, object-based), and
Predictability (blocked and mixed) as within-subjects factors. The main effect of Cueing was
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significant, F (1, 20) = 20.756; p < .001; ηp2 = .509, reflecting IOR. The main effect of Target
Type was significant, F (2, 40) = 118.452; p < .001; ηp2 = .856, reflecting faster RTs for motion
trials. The main effect of Predictability was also significant, F (1, 20) = 7.640; p < .012; ηp2 =
.276, reflecting faster RTs in the blocked condition. Target Type and Cueing showed a significant
interaction, F (2, 40) = 8.817; p < .001; ηp2 = .306, again reflecting that IOR was present in no
motion trials (t (20) = 4.871; p < .001), marginally significant in location-based coordinates (t
(20) = 1.996; p = .060), and not significant in object-based coordinates (t (20) < 1). Predictability
and Target Type also qualified for an interaction, F (2, 40) = 5.997; p < .005; ηp2 =.231,
reflecting that RTs on no motion trials in the mixed condition were slower than in the blocked
condition. The interaction of Predictability and Cueing and the three-way interaction were not
significant (F < 1).
In summary, Experiment 2 revealed significant IOR in the no motion condition, but this
IOR effect was eliminated when the objects moved, especially in the blocked condition. In the
mixed condition, there was a small but significant location-based IOR effect remaining when the
objects moved, but there was no evidence of object-based IOR. The no motion condition
produced overall slower RTs than when the objects moved, probably because the object motion
acted as an additional temporal signal that the target was about to appear. It is unlikely that IOR
was diminished in motion trials due to fast RTs alone, however, because RTs were no faster than
in Experiment 1, in which reliable IOR was obtained.
Experiments 1 and 2 together suggest that inhibitory tags are automatically updated into
spatiotopic coordinates across eye movements, but they are not attached to an object shifting to a
similar extent and with similar timing when the motion of the object across the retina is
generated externally instead of internally. To directly assess the differences between internally-
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
19
and externally-generated motion we compared the saccade trials in Experiment 1a and the
blocked motion condition of Experiment 2. We chose to compare these two conditions in
particular because they are matched in terms of the predictability of changes on the retina, with
the only difference between them being whether the motion is due to a predictable eye movement
or due to the objects themselves shifting in a predictable direction.
Comparison of Experiment 1a and 2. A 2x2x2 mixed measures ANOVA with Cueing (cued and
uncued) and Reference Frame (retinotopic/ location-based and spatiotopic/ object-based) as
within-subject factors and Experiment (Experiment 1a and 2) as the between subjects factor was
conducted. The analysis revealed a main effect of Cueing, F (1, 44) = 8.678; p < .005; ηp2 = .165.
The main effect of Reference Frame was also significant, F (1, 44) = 5.139; p < .05; ηp2 = .105,
reflecting that targets in the spatiotopic reference frame had larger RTs. Cueing and Experiment
qualified for an interaction; F (1, 44) = 4.477; p <.05; ηp2=.092; reflecting that IOR was present
across eye movements, but not across object motion. No other interactions were significant.
The analysis confirmed that the IOR effect was present in the eye movement condition,
but eliminated in the predictable object motion condition. Despite the similarities of the changes
on the retina and the predictability of these changes, IOR was maintained across self-generated
motion, but not across externally-produced motion.
General Discussion
The present study examined the impact of eye movements and object motion on IOR to
establish whether a general prediction-based mechanism facilitates the transfer of inhibitory tags
into spatiotopic coordinates across eye movements (E1a and E1b) and into object-based
coordinates across object motion (E2). The findings show that IOR is maintained across
saccades, in both retinotopic and spatiotopic coordinates, regardless of whether the observer has
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
20
foreknowledge of the direction of an upcoming eye movement. In contrast, and under similar
conditions, IOR was eliminated by the external motion of objects compared to trials where no
motion occurred. There was no evidence that the IOR effect shifted with a moving object, even
when the direction and size of the object’s motion was perfectly predictable. Direct comparison
of the eye movement condition and the object motion condition confirmed that IOR is
maintained across self-generated retinal motion but eliminated across object motion. The
implications of these findings are discussed below.
IOR across Eye Movements
The current study confirmed that IOR can be reliably observed in the spatiotopic location
of cues when a saccade intervenes between the cue and target onset. As such, the study offers
further support that IOR represents a bias of attention towards novelty that facilitates visual
search (Klein & MacInnes, 1999). However, it is important to note that, like several other studies
to date (Abrams & Pratt, 2000; Mathot & Theeuwes, 2010; Pertzov et al., 2010; Sapir et al.,
2004), we also found evidence that IOR is retinotopic. The difference in magnitude between
spatiotopic and retinotopic IOR was not statistically significant, but it was numerically smaller in
retinotopic than in spatiotopic coordinates, which is similar to trends in previous studies (Abrams
& Pratt; Pertzov et al.; Sapir et al.). It is possible that restricted laboratory conditions in this and
other standard cue-target paradigms encourages the presence of retinotopic IOR. Cue-target
paradigms are, unlike real world sceneries, often highly simplified and symmetric. Perhaps the
transfer from the originally retinotopic location of the inhibition (before the eye movement) is
not a complete process and traces of the retinotopic inhibition remain activated by the
imperfection of the orienting mechanism. In real world situations such as free visual search,
other factors may overcome the retinotopic inhibition (such as search strategies and a richer and
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
21
more variable scene layout) and therefore the need to fully clear the “retinotopic buffer” of the
inhibition may be small.
Previous studies have indicated that the reference frame of IOR depends on a number of
parameters, such as the nature of the interfering eye movement (Abrams & Pratt, 2000) and the
extent of featural salience of the stimuli (Hilchey et al., 2012). As such, predictability might have
been expected to play a role in facilitating the updating of inhibition into spatiotopic coordinates.
However, our findings showed that spatiotopic IOR occurred regardless of whether the upcoming
eye movement direction could be predicted with certainty at the time of the onset of the
exogenous cue. This suggests a rapid, involuntary mechanism that remaps inhibitory tags into
spatiotopic coordinates across saccades, consistent with saccadic remapping.
Location-based and object-based IOR
We measured the allocation of IOR across blocked and randomly interleaved object
motion conditions to investigate whether the presence or strength of object-based IOR would
depend on the ability to predict an object’s upcoming motion with certainty. We only observed
consistent IOR in trials when the objects did not move; small but significant location-based IOR
was observed on trials where the objects moved in unpredictable directions, that is, in the mixed
rather than blocked conditions. This is perhaps surprising, because the blocked condition might
have been expected to produce more robust IOR than the mixed condition, given that blocking
the motion direction allows observers to predict the future location of the cued object, which
better matches the eye movement condition, in which robust IOR was observed. . However, a
decrease in the magnitude of IOR following sudden changes in the search environment has been
observed previously (e.g. MacInnes & Klein, 2003). Perhaps having the foreknowledge that the
objects will move, which observers would only have in the blocked condition, led to an
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
22
attenuation of the IOR effect relative to the mixed condition, in which the objects may or may
not move on any given trial.
Our findings stand in contrast to previous reports of IOR that is attached to moving
objects (e.g. Tipper et al., 1991). However, it is not unprecedented to observe IOR in locationbased coordinates across object-motion (Abrams & Pratt, 2000; Müller & von Mühlenen, 1996),
and the current design and that of Tipper et al. differ in many aspects. For example, our objects
shifted abruptly from one location to another, rather than moving smoothly as in Tipper et al.. It
is possible that the visual system treats sudden motion as a scene change and therefore clears the
‘inhibitory buffer’, as MacInnes and Klein (2003) reported. It is an interesting and open question
whether the type of object motion can influence the robustness of object-based IOR. That said,
we specifically used sudden object shifts in Experiment 2 to better match the sudden changes
that occur on the retina across eye movements that would have been produced in Experiment 1.
Direct comparison of the eye movement and object motion condition confirmed that IOR is
eliminated across predictable object motion but maintained across eye movements. As such, the
current study illustrates the importance of the efference copy signal in maintaining inhibitory
tags in locations in space across eye movements: IOR was automatically updated into spatiotopic
coordinates across eye movements, but not into object-based coordinates, even across highly
predictable object motion. This suggests that predictability alone is not sufficient for the updating
of inhibitory tags in dynamic environments and across changing retinotopic maps, supporting the
notion that efference copy is a necessary precursor for updating visual space (or visual attention
within this space, Cavanagh, Hunt, Afraz & Rolfs, 2010). The suggestion (Abrams & Pratt;
Pertzov et al., 2010, Sapir et al., 2004) that the retinotopic locations of inhibitory tags are
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
23
updated rapidly and automatically with each eye movement is thus further supported by the
current findings.
Conclusion
In Experiment 1 we showed that IOR across eye movements is maintained in both
retinotopic and spatiotopic reference frames, irrespective of whether the upcoming eye
movement direction can be predicted with certainty. In Experiment 2, which matched the
conditions of Experiment 1 except in the respect that the objects moved rather than the eyes,
object-based IOR was not observed. These results suggest the maintenance of inhibitory tags in
spatiotopic coordinates across saccades is an automatic process, likely to be supported by an
efferent signal from the oculomotor motor system. The results also support the idea that IOR
reflects an inhibitory tagging mechanism that can orient attention towards novel locations during
active, overt scanning of the visual environment.
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
24
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Table 1. Summary of the saccadic information of Experiment 1a and 1b
Experiment 1a
Experiment 1b
Latency
STOA
STI
Latency
STOA
STI
Before
266.16
533.84
428.59
418.29
381.71
290.12
Exclusion
(18.1)
(18.8)
(18.4)
(12.6)
(12.6)
(10.32)
After
262.92
537.11
435.64
392.27
407.73
317.12
Exclusion
(14.4)
(14.37)
(13.1)
(12.24)
(12.2)
(5.3)
Note. The mean saccadic latency, saccade to target onset asynchrony (STOA) and saccade
to target interval (STI) before and after exclusions of extreme STI (<180, >700). Values in
brackets denote the standard error of the mean.
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
Table 2. The mean reaction times and standard deviations (in brackets) in Experiment
1a and 1b.
Experiment 1a
uncued
Experiment 1b
Target type
cued
cued
No motion
333.5 (42.2)
321.5 (41.7)
314.1 (37.0)
305.9 (39.3)
Retinotopic
336.7 (46.5)
328.6 (49.4)
304.1 (39.6)
298.3 (45.5)
Spatiotopic
342.5 (51.6)
331.3 (49.5)
309.9 (36.3)
302.8 (41.5)
Note. All cued/uncued pairs differed significantly from each other.
Uncued
29
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
30
Table 3. The mean reaction times and standard deviations (in brackets) in Experiment 2
Experiment 2
Blocked
Target type
cued
No motion
366.6 (92.4)
Location-based
Object-based
Mixed
uncued
cued
uncued
349.5 (86.5) **
394.0 (65.4)
381.9 (71.2)
*
315.6 (58.6)
311.6 (62.7)
325.4 (65.7)
318.6 (67)
*
319.5 (59.5)
319.1 (60.4)
324.1 (62.7)
328.3 (61.9)
Note. Pairs of cued and uncued targets that differed significantly from each other are in boldface
((*)p<.1, two tailed. *p<.05, two-tailed. **p<.001, two-tailed.).
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
Figure 1. A schematic representation of Experiment 1. Examples of a
spatiotopic and retinotopic target are shown for an eye movement to the
right.
31
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
IOR (cued-uncued) in ms
IOR (cued-uncued) in ms
Object motion
Eye movements
Blocked
32
Mixed
25
25
20
20
15
15
10
10
5
5
0
0
-5
-5
-10
-10
25
25
20
20
15
15
10
10
5
5
0
0
-5
-5
-10
-10
No Saccade
Retinotopic
Spatiotopic
No Motion
Location-based
Object-based
Figure 2. IOR (cued-uncued RT) for four different target types in Experiment 1a (top left),
Experiment 1b (top right), Experiment 2 blocked (bottom left) and Experiment 2 mixed (bottom
right). IOR was significant when no motion occurred (dark gray) and across all target types when
an eye movement was made (top row). However, no object-based IOR was observed (bottom
row). Error bars indicate within subject variability in the 95% confidence interval (Cousineau,
2005).
INHIBITION OF RETURN ACROSS EYE AND OBJECT MOVEMENTS
Figure 3. Schematic representation of Experiment 2 trial events. In the
example above the objects shifts to the left and the location-based (left) and
object-based (right) target locations are shown.
33